(Mis)understanding mirror neurons

This may be a bit technical for many MindBlog readers, but Hickok and Hauser offer a simple, succinct, and incisive critique of the current dogma about mirror neurons that is sufficiently important that I would like to pass it on.  They suggest, as an alternative to the common assumption that mirror neurons are involved in action understanding, that their activity instead might reflect sensory-motor learning. They illustrate this distinction with a simple graphic (in which ventral stream refers to pathways moving more through the temporal lobe of the brain - the 'what' pathway, with dorsal stream routing more through the parietal lobe - the 'where' pathway. Both pathways converge in pre-motor cortical areas such as F5):

Summary
It is hard to imagine a class of neurons that has generated more excitement than mirror neurons, cells discovered by Rizzolatti and colleagues [1] in macaque area F5 that fire both during action execution and action observation. We suggest, however, that the interpretation of mirror neurons as supporting action understanding was a wrong turn at the start, and that a more appropriate interpretation was lying in wait with respect to sensorimotor learning. We make a number of arguments, as follows. Given their previous work, it would have been natural for Rizzolatti's group to interpret mirror neurons as involved in action selection rather than action understanding. They did not make this assumption because, at the time, the data suggested that monkey behavior did not support such an interpretation. Recent evidence shows that monkeys do, in fact, exhibit behaviors that support this alternative interpretation. Thus, the original basis for claiming that mirror neurons mediate action understanding is no longer compelling. There are independent arguments against the action understanding claim and in support of a sensorimotor learning origin for mirror neurons. Therefore, the action understanding theory of mirror neuron function requires serious reconsideration, if not abandonment.
Main Text
Mirror neurons were discovered in the context of research aimed at understanding how the visual properties of objects are integrated with motor codes for action. Cells in area F5 were found to respond to visually presented objects as well as during grasping actions towards those objects. The interpretation of this circuit was that it coded a “vocabulary of motor acts and that this vocabulary can be accessed by … visual stimuli” (p. 491) [2] and that it was critical for “learning associations, including arbitrary associations between stimuli and [motor] schemas” (p. 317) [3]. This is a “‘pragmatic’ mode of processing, the function of which is to extract parameters that are relevant to action, and to generate the corresponding motor commands” (p. 320), as opposed to “‘semantic’ analysis [which is] performed in the temporal lobe” (p.314) [3]. Thus, the meaning of objects is not coded in F5, although clearly, “the semantic system can influence the pragmatic system” (p. 320) [3] (for example, we want to reach for food not snakes).

Mirror neurons were discovered within this same circuit and found to have similar sensorimotor properties [1,4]. It was even suggested that “the actions performed by other monkeys must be a very important factor in determining action selection” (p. 179) [4] and that “the [motor] vocabulary of F5 can be addressed in two ways: by objects and by events [actions]” (p. 317) [3]. Thus, the theoretical and empirical pieces were in place to interpret mirror neurons as sensorimotor association cells relevant to action selection, just like object-oriented cells (Figure 1). But this interpretation was not considered — why?

Figure 1 (click to enlarge)
Schematic models of dorsal and ventral stream function.
(A) The current dominant model [1], which holds that object- and action-oriented processes for sensorimotor integration and ‘understanding’ are organized differentially, with action understanding part of the dorsal sensorimotor stream and object ‘understanding’ part of the ventral stream. (B) A more conventional model in which object- and action-oriented processes for sensory-motor integration and understanding are organized similarly. Both models assume that semantic information from the ventral stream can modulate sensorimotor processes in the dorsal stream.

It was the mirroring property of mirror neurons that steered investigators away from a straightforward sensorimotor interpretation. The logic was, if mirror actions (for example, imitation) are not in the species' repertoire, then mirror neurons can have no motor selection function. Rizzolatti and Craighero used this argument, pitting “two main hypotheses” of mirror neuron function, imitation and action understanding; because macaques do not imitate, they argued, mirror neurons must support action understanding (p. 172) [1]. However, these authors, and the field generally, have failed to notice that other forms of mirror actions are in the macaque motor repertoire. For example, field studies show that rhesus monkeys perceive human gestures as goal-directed, including those that mimic the rhesus monkeys' species-specific signal for coalition recruitment [5]. Macaques also engage in contagious yawning, where perception of another's yawn triggers a yawn in the observer [6]. Further, experimental work has found that another's grasping actions toward one of two food receptacles serves as a cue to goal-directed grasping toward that same receptacle [7] — an experimental situation reminiscent of the mirror neuron studies. Even domesticated dogs mirror goal-directed actions of a model dog [8]; one would expect to find mirror neurons in dogs given this behavioral evidence. And lastly, rhesus monkeys comprehend actions that they are physically incapable of producing. In particular, though rhesus monkeys do not throw, they can recognize a throwing action in humans, realizing that throwing a rock is dangerous whereas throwing food is not [5].

Observed actions can serve as important inputs to action selection, including, but not necessarily limited to, mirror actions. Therefore, the motivating argument for the action understanding theory over a sensorimotor theory (for example [9]) does not hold.

Can we distinguish the sensorimotor and action understanding theories of mirror neurons? Yes: empirical findings favor the sensorimotor account by showing that action understanding and motor system function dissociate [10], that motor actions alone are insufficient to explain action understanding [5], that animals comprehend many actions that they cannot execute [10], and that sensorimotor learning can transform the mirror system [9].

In summary, a sensorimotor theory can explain the response properties of mirror neurons, does so more straightforwardly, and does not suffer the empirical roadblocks of the action understanding theory [5,10]. It is time to reconsider mirror neuron function and the neural basis of action understanding.

References
1 Rizzolatti, G., and Craighero, L. (2004). The mirror-neuron system. Annu. Rev. Neurosci. 27, 169–192.
2 Rizzolatti, G., Camarda, R., Fogassi, L., Gentilucci, M., Luppino, G., and Matelli, M. (1988). Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp. Brain Res. 71, 491–507.
3 Jeannerod, M., Arbib, M.A., Rizzolatti, G., and Sakata, H. (1995). Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci. 18, 314–320.
4 di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., and Rizzolatti, G. (1992). Understanding motor events: a neurophysiological study. Exp. Brain Res. 91, 176–180.
5 Hauser, M., and Wood, J. (2010). Evolving the capacity to understand actions, intentions, and goals. Annu. Rev. Psychol 61, 303–324, C301.
6 Paukner, A., and Anderson, J.R. (2006). Video-induced yawning in stumptail macaques (Macaca arctoides). Biol. Lett. 2, 36–38.
7 Wood, J.N., Glynn, D.D., Phillips, B.C., and Hauser, M.D. (2007). The perception of rational, goal-directed action in nonhuman primates. Science 317, 1402–1405.
8 Range, F., Viranyi, Z., and Huber, L. (2007). Selective imitation in domestic dogs. Curr. Biol. 17, 868–872.
9 Heyes, C. (2010). Where do mirror neurons come from?. Neurosci. Biobehav. Rev. 34, 575–583.
10 Hickok, G. (2009). Eight problems for the mirror neuron theory of action understanding in monkeys and humans. J. Cogn. Neurosci. 21, 1229–1243.

Reciprocity engages our brain's reward system.

Interesting stuff from Phan et al:

Brain reward circuitry, including ventral striatum and orbitofrontal cortex, has been independently implicated in preferences for fair and cooperative outcomes as well as learning of reputations. Using functional MRI (fMRI) and a “trust game” task involving iterative exchanges with fictive partners who acquire different reputations for reciprocity, we measured brain responses in 36 healthy adults when positive actions (entrust investment to partners) yield positive returns (reciprocity) and how these brain responses are modulated by partner reputation for repayment. Here we show that positive reciprocity robustly engages the ventral striatum and orbitofrontal cortex. Moreover, this signal of reciprocity in the ventral striatum appears selectively in response to partners who have consistently returned the investment (e.g., a reputation for reciprocity) and is absent for partners who lack a reputation for reciprocity. These findings elucidate a fundamental brain mechanism, via reward-related neural substrates, by which human cooperative relationships are initiated and sustained.

Nuturing robots

A recent article by Benedict Carey suggests we may be heading towards a future in which instructional and emotional needs of those not able to obtain appropriate human contact are met through presentation of changing robotic emotional expressions that activate the same brain areas as normal human gestures. A report by Chaminade et al., however, on a multi-national collaboration involving the humanoid robot WE4-RII - which expresses emotions by using facial expressions and the movement of the upper-half of the body including neck, shoulders, trunk, waist, as well as arms and hands - suggests that we have some way to go:

...activity in cortical areas endowed with mirror properties, like left Broca's area for the perception of speech, and in the processing of emotions like the left anterior insula for the perception of disgust and the orbitofrontal cortex for the perception of anger, is reduced for robot stimuli, suggesting lesser resonance with the mechanical agent. Finally, instructions to explicitly attend to the emotion significantly increased response to robot, but not human facial expressions in the anterior part of the left inferior frontal gyrus, a neural marker of motor resonance.

The Carey article reviews a number of different robotic instructional studies that show, in spite of the attenuated effectiveness of robotic versus human emotions, that robots can engage people and teach them simple skills, including household tasks, vocabulary or, in the case of autistic children, playing, elementary imitation and taking turns.

Mind reading - How to seem telepathic

Here I attempt to summarize  an article by Eyai and Epley (on enabling mind reading by matching construal levels) by patching together bits of abstract and body text.  The results make the point that accurately reading other minds to know how one is evaluated by others—or how others evaluate themselves—requires focusing one’s evaluative lens at the right level of detail:

People can have difficulty intuiting what others think about them at least partly because people evaluate themselves in more fine-grained detail than observers do. This mismatch in the level of detail at which people construe themselves versus others diminishes accuracy in social judgment. Being a more accurate mind reader requires thinking of oneself at a higher level of construal that matches the observer’s construal (Experiments 1 and 2)*, and this strategy is shown in a further experiment (experiment 4**) to be more effective in this context than perspective taking (putting oneself in other people's shoes).

*Experiment 1 involved predicting judgements of attractiveness. This experiment found subjects to be more accurate in intuiting how attractive they will be judged (by others viewing a recent photo of themselves) in the distant future than in the near future. Experiment 2 involved predicting overall impression of oneself that observers would gain from listening (in the near versus distant future) to a recording they made on various topics. Again, predictions were more accurate for the imagined distant future. Thus altering construal level (near versus distant future) can increase accuracy in two very common and important instances of mind reading in everyday life—intuiting how attractively one will be evaluated by others and intuiting others’ overall impressions of oneself.

Accurately intuiting how others evaluate themselves requires the opposite strategy—thinking about others in a lower level of construal that matches the way people evaluate themselves. **In Experiment 4, University of Chicago undergraduates (N = 62) participated in a procedure similar to that of Experiment 1, except that targets rated how attractive they found themselves, using a scale ranging from 1 (not at all) to 9 (very), and observers received the construal manipulation. Observers were told that the pictures were taken earlier in the day (near condition) or a few months earlier (distant condition), and rated how attractive they thought the targets found themselves to be, using the same scale. Observers were more accurate in the near than in the distant condition.

Speech perception requires motor system activation.

Yuen et al. find that specific articulatory commands are activated automatically and involuntarily during speech perception, and suggest, in a broader framework, that perception of action entails activation of the motor system. Their behavioral evidence backs up functional MRI studies that have demonstrated that the brain regions involved in the perception of speech overlap with those involved in the production of speech. They reasoned that if articulatory information is activated in speech perception, then this information should interfere with articulation in a scenario in which participants are asked to produce a target syllable while listening to a different auditory distractor. Their approach was to investigate how an auditory distractor impacts upon the actual articulation of a different target. The thought was that if articulatory information is activated in speech perception, then that information might interfere with speech production by introducing particular distortions of the target syllable that reflect the articulatory properties of the distractor. Here is their abstract:

Emerging neurophysiologic evidence indicates that motor systems are activated during the perception of speech, but whether this activity reflects basic processes underlying speech perception remains a matter of considerable debate. Our contribution to this debate is to report direct behavioral evidence that specific articulatory commands are activated automatically and involuntarily during speech perception. We used electropalatography to measure whether motor information activated from spoken distractors would yield specific distortions on the articulation of printed target syllables. Participants produced target syllables beginning with /k/ or /s/ while listening to the same syllables or to incongruent rhyming syllables beginning with /t/. Tongue–palate contact for target productions was measured during the articulatory closure of /k/ and during the frication of /s/. Results revealed “traces” of the incongruent distractors on target productions, with the incongruent /t/-initial distractors inducing greater alveolar contact in the articulation of /k/ and /s/ than the congruent distractors. Two further experiments established that (i) the nature of this interference effect is dependent specifically on the articulatory properties of the spoken distractors; and (ii) this interference effect is unique to spoken distractors and does not arise when distractors are presented in printed form. Results are discussed in terms of a broader emerging framework concerning the relationship between perception and action, whereby the perception of action entails activation of the motor system.

The fMRI of understanding others' regret.

Rizzolatti and colleagues carry the mirror neuron story to an even higher level in a study of regret:

Previous studies showed that the understanding of others' basic emotional experiences is based on a “resonant” mechanism, i.e., on the reactivation, in the observer's brain, of the cerebral areas associated with those experiences. The present study aimed to investigate whether the same neural mechanism is activated both when experiencing and attending complex, cognitively-generated, emotions. A gambling task and functional-Magnetic-Resonance-Imaging (fMRI) were used to test this hypothesis using regret, the negative cognitively-based emotion resulting from an unfavorable counterfactual comparison between the outcomes of chosen and discarded options. Do the same brain structures that mediate the experience of regret become active in the observation of situations eliciting regret in another individual? Here we show that observing the regretful outcomes of someone else's choices activates the same regions that are activated during a first-person experience of regret, i.e. the ventromedial prefrontal cortex, anterior cingulate cortex and hippocampus. These results extend the possible role of a mirror-like mechanism beyond basic emotions.

Origins of empathetic yawning?

Interesting observations by Palagi et al:

Yawn contagion in humans has been proposed to be related to our capacity for empathy. It is presently unclear whether this capacity is uniquely human or shared with other primates, especially monkeys. Here, we show that in gelada baboons (Theropithecus gelada) yawning is contagious between individuals, especially those that are socially close, i.e., the contagiousness of yawning correlated with the level of grooming contact between individuals. This correlation persisted after controlling for the effect of spatial association. Thus, emotional proximity rather than spatial proximity best predicts yawn contagion. Adult females showed precise matching of different yawning types, which suggests a mirroring mechanism that activates shared representations. The present study also suggests that females have an enhanced sensitivity and emotional tuning toward companions. These findings are consistent with the view that contagious yawning reveals an emotional connection between individuals. This phenomenon, here demonstrated in monkeys, could be a building block for full-blown empathy.

Three different yawning displays performed by gelada baboons. Covered teeth yawning (left) uncovered teeth yawning (middle). and uncovered gums yawning (right).

Monkeys affiliate with humans who imitate them.

It is generally thought that imitation is one mechanism through which cultural learning occurs. When others mimic us, we like them more, empathize with them more, and are more helpful and generous toward them. Recent work with capuchin monkeys suggests that imitation may of general importance in enhancing prosocial social behaviors, suggesting that the social consequences of mimicry may have deeper evolutionary roots than previously thought. Paukner et al. find that these animals behave in a more affiliative manner, as assessed by direction of gaze, physical proximity, and token exchange, toward humans who imitate them as compared to humans who perform the same movements, but not at the same time.

Racial group membership modulates empathic brain responses.

From Xu et al.:

The pain matrix including the anterior cingulate cortex (ACC) mediates not only first person pain experience but also empathy for others' pain. It remains unknown, however, whether empathic neural responses of the pain matrix are modulated by racial in-group/out-group relationship. Using functional magnetic resonance imaging we demonstrate that, whereas painful stimulations applied to racial in-group faces induced increased activations in the ACC and inferior frontal/insula cortex in both Caucasians and Chinese, the empathic neural response in the ACC decreased significantly when participants viewed faces of other races. Our findings uncover neural mechanisms of an empathic bias toward racial in-group members.


Figure - a, Illustration of Caucasian faces receiving painful and non-painful stimuli. b, Illustration of Chinese faces receiving painful and non-painful stimuli. c, Contrast values of the parameter estimates of signal intensity in the ACC and the frontal cortex that differentiated painful and non-painful stimuli in Caucasians. d, Contrast values of the parameter estimates of signal intensity in the ACC and the frontal cortex that differentiated painful and non-painful stimuli in Chinese. e, Correlation between ACC empathic neural responses to racial in-group and out-group members. X and Y axes respectively indicate ACC empathic responses to racial in-group and racial out-group members indexed in contrast values of painful versus non-painful stimulation. f, Increased activations in the ACC and the frontal/insula cortex shown in whole-brain statistical parametric mapping analyses when participants perceived racial in-group faces. The upper figures show the results from Caucasian subjects and the lower figures show the results from Chinese subjects.

The synchronization of brains

A relevant follow up to the recent posts on Metzinger's book, which discussed the synchronization of our 'ego tunnels': Bharucha suggests that understanding of how brains synchronize — or fail to do so — will be a game-changing scientific development.

No evidence for mirror neurons in humans?!

Given all the hype over the mirror neuron system in humans (basis for constructing social cognition, empathy, mind reading, and the development of language, etc. - this blog has mostly joined the chorus) , this recent work by Lingnau would seem to be quite a bombshell. Their introduction explains the logic, context and basic results:

There are 2 conditions that must be fulfilled by any study that aims to address the existence of mirror neurons in humans. First, it must be demonstrated that execution and recognition of a specific motor act activate a common set of neurons in so-called mirror neuron areas (condition I). Importantly, this overlap must be act specific. Second, it must be demonstrated that activation of neurons within potential mirror neuron areas results from direct activation and not from a prior nonmotor categorization on the basis of inferences about potential motor acts from minimal visual cues, e.g., seeing a hand move toward a familiar graspable object, inviting the inference that the actor's intention may be to grasp the object (condition II).

Their study meets these conditions:

We studied within- and cross-modal adaptation for simple intransitive motor acts that are not associated with a particular meaning, such that any observed adaptation effect could not be attributed to adaptation of the same semantic representation or the same object. Furthermore, to ensure that participants would not be able to guess the target motor act from initial features of a movement, we used 8 different unpredictable movements that could be distinguished from each other only at a relatively late phase of the movement.

We found adaptation for executed motor acts, when these were preceded by execution or observation of the same motor act, as would be expected if a previously executed or observed motor act were to prime the subsequent execution of that act. Importantly, we found no sign of adaptation when motor acts were first executed and then observed. ...our data do not support the direct matching account, according to which neurons exist that selectively respond to actions irrespective of whether these are observed or executed. Our data are compatible with the assumption that responses in mirror neuron areas reflect the facilitation of the motor system because of learned associations between semantic representation of actions and their generating motor programs.

Ramachandran and the plastic brain.

John Colapinto writes a New Yorker article on Vilayanur Ramachandran, whose work I have mentioned several times (actually, in six postings...enter Ramachandran in the search box in the left column to bring them up.) It is a biographical account, describing Ramachandran's professional development, and also describes an interesting syndrome known as apotemnophilia, the compulsion to have a healthy limb amputated. It appears to result from damage to the right superior parietal lobe which causes it to fail in assembling a normal body image for the body part perceived as alien, wanting amputation. Just as was the case with phantom limb pain and stroke induced paralysis, Ramachandran found that use of a simple mirror to differently present a body part could alleviate the symptoms. The article also describes work which suggests a link between autism and defects in the mirror neuron system.

I feel what you feel if we are similar

From Serino et al.:

Social interactions are influenced by the perception of others as similar or dissimilar to the self. Such judgements could depend on physical and semantic characteristics, such as membership in an ethnic or political group. In the present study we tested whether social representations of the self and of others could affect the perception of touch. To this aim, we assessed tactile perception on the face when subjects observed a face being touched by fingers. In different conditions we manipulated the identity of the shown face. In a first experiment, Caucasian and Maghrebian (Northern African) participants viewed a face belonging either to their own or to a different ethnic group; in a second experiment, Liberal and Conservative politically active participants viewed faces of politicians belonging to their own or to the opposite political party. The results showed that viewing a touched face most strongly enhanced the perception of touch on the observer's face when the observed face belonged to his/her own ethnic or political group.

Ramachandran on qualia and the self.

His bottom line, in an essay in Edge, is that the Qualia problem (how can a martian that knows every physical wiring detail of my seeing red actually have my experience of red) is a pseudo-problem, like two sides of a Moebius strip that look utterly different from our ant-like perspective but are in reality a single surface. From his essay:

The problem of self, on the other hand, is an empirical one that can be solved—or at least explored to its very limit—by science. If and when we do it will be a turning point in the history of science. Neurological conditions have shown that the self is not the monolithic entity it believes itself to be. It seems to consist of many components each of which can be studied individually, and the notion of one unitary self may well be an illusion. (But if so we need to ask how the illusion arises; was it an adaptation acquired through natural selection?)

Ramachandran then goes on to describe the fascinating variations in our sense of self that can be correlated with brain changes. In a previous essay on mirror neurons he

...speculated that these neurons can not only help simulate other people's behavior but can be turned "inward"—as it were—to create second-order representations or metarepresentations of your own earlier brain processes. This could be the neural basis of introspection, and of the reciprocity of self awareness and other awareness. There is obviously a chicken-or-egg question here as to which evolved first, but that is tangential to my main argument.... The main point is that the two co-evolved, mutually enriching each other to create the mature representation of self that characterizes modern humans. Our ordinary language illustrates this, as when we say "I feel a bit self conscious", when I really mean that I am conscious of others being conscious of me. Or when I speak of being self critical or experiencing "self-pity". (A chimp could—arguably—feel pity for a begging chimp, but I doubt whether it would ever experience self-pity.)

I also suggest that although these neurons initially emerged in our ancestors to adopt another's allocentric visual point of view, they evolved further in humans to enable the adoption of another's metaphorical point of view. ("I see it from his point of view" etc.) This, too, might have been a turning point in evolution although how it might have occurred is deeply puzzling.

La gazza ladra passes the mirror test - a crow with a self!

The Eurasian magpie belongs to the same bird family that includes the crows, ravens, and jays. de Waal writes a fascinating review of recent work by Prior et al. that demonstrates that magpies recognize themselves in a mirror - a test that persists as the gold standard of self-identity or 'personhood.' The experiments actually had better controls than many of those done with apes and human children...

...which generally fail to include “sham” marks. A sham mark is applied in the same way as a visible mark, and supposed to feel and smell the same, but cannot be visibly detected. In the magpie study, this was done by placing a black mark onto the magpies' black throat feathers.

Placed on the same black throat feathers, the visible mark—a tiny colored sticker—stood out, but only in a mirror. Put in front of a mirror, the magpies kept scratching with their foot until the mark was gone, whereas they left the sham mark alone. They also didn't do the same amount of frantic scratching if there was no mirror to see themselves in. Evidently, their self-preening was guided by visual feedback from the mirror.

de Waal also discusses work with other species and the “co-emergence hypothesis,” according to which the capacities for mirror self recognition and perspective-taking appear in tandem during both evolution and development.

Speaking of crows, Nijhuis writes a brief piece on work showing that crows recognize individual human faces.

Our relationship with mirrors...

Natalie Angier offers an excellent discussion of the biology, psychology and physics of our relationship with mirrors, how they are used in studies of self awareness in humans and animals, and also in treating disorders like phantom limb syndrome, chronic pain and post-stroke paralysis. I show here a nice graphic from the article explaining why few of us understand how our mirrors images really work.

Do chimpanzees have a theory of mind? 30 years later

Call and Tomasello offer a review in the May issue of Trends in Neuroscience on the controversial question of how much our nearest relatives understand about the minds of others:

On the 30th anniversary of Premack and Woodruff's seminal paper asking whether chimpanzees have a theory of mind, we review recent evidence that suggests in many respects they do, whereas in other respects they might not. Specifically, there is solid evidence from several different experimental paradigms that chimpanzees understand the goals and intentions of others, as well as the perception and knowledge of others. Nevertheless, despite several seemingly valid attempts, there is currently no evidence that chimpanzees understand false beliefs. Our conclusion for the moment is, thus, that chimpanzees understand others in terms of a perception–goal psychology, as opposed to a full-fledged, human-like belief–desire psychology.

Here is one description of an experimen showing that Chimpanzees infer a human's intentions:

Buttelmann et al. [Dev. Sci. 10 (2007 pp. F31–F38]...tested six human-raised chimpanzees in the so-called rational-imitation paradigm. The chimpanzees were shown how to operate an apparatus to produce an interesting result (e.g. lights or sounds), and then they were given a turn. The most natural behavior for them in all cases was to operate it with their hands. But this obvious behavior was never demonstrated for them; they always saw a human manipulate the apparatus in a novel way with some other body part. The idea was that in some cases the physical constraints of the situation dictated that the human (referred to as ‘E’ in the figure) had to use that unusual body part; for example, he had to turn on a light with his head because his hands were occupied holding a blanket or he had to operate a light with his foot because his hands were occupied with a heavy bucket (see Figure I). When the chimpanzees saw this forced use of the unusual body part, they mostly discounted it and used their hands as they normally would (because the constraints were not present for them). However, when they saw the human use the unusual body part when there was no physical constraint dictating this, they quite often copied the unusual behavioral means themselves. If we interpret this experiment the way it is interpreted for human infants, the conclusion is that the chimpanzees understood not only what the experimenter was trying to do (his goal) but also why he was doing it in the way he was doing it – the rationality behind the choice of the plan of action toward the goal. According to Tomasello et al. [Behav. Brain Sci. 28 (2005), pp. 675–691], an understanding of the action plan chosen toward a goal constitutes an understanding of the intention.

Regulating the brain circuits of compassion

Here is yet more compelling evidence that you are what you spend your time imagining. In a recent study in PLoS ONE, Lutz, Davidson and colleagues extend their previous work on correlations between brain states and meditation to show that one particular kind of Buddhist meditation, which emphasizes empathetic and loving thoughts towards others and self, changes the brain's reactivity to emotional sounds. In experienced practitioners of the 'loving-kindness-compassion' meditation technique, such images caused larger reactions in the insular and anterior cingulate cortices than were observed in novices. Here is their abstract and one figure from the paper.

Recent brain imaging studies using functional magnetic resonance imaging (fMRI) have implicated insula and anterior cingulate cortices in the empathic response to another's pain. However, virtually nothing is known about the impact of the voluntary generation of compassion on this network. To investigate these questions we assessed brain activity using fMRI while novice and expert meditation practitioners generated a loving-kindness-compassion meditation state. To probe affective reactivity, we presented emotional and neutral sounds during the meditation and comparison periods. Our main hypothesis was that the concern for others cultivated during this form of meditation enhances affective processing, in particular in response to sounds of distress, and that this response to emotional sounds is modulated by the degree of meditation training. The presentation of the emotional sounds was associated with increased pupil diameter and activation of limbic regions (insula and cingulate cortices) during meditation (versus rest). During meditation, activation in insula was greater during presentation of negative sounds than positive or neutral sounds in expert than it was in novice meditators. The strength of activation in insula was also associated with self-reported intensity of the meditation for both groups. These results support the role of the limbic circuitry in emotion sharing. The comparison between meditation vs. rest states between experts and novices also showed increased activation in amygdala, right temporo-parietal junction (TPJ), and right posterior superior temporal sulcus (pSTS) in response to all sounds, suggesting, greater detection of the emotional sounds, and enhanced mentation in response to emotional human vocalizations for experts than novices during meditation. Together these data indicate that the mental expertise to cultivate positive emotion alters the activation of circuitries previously linked to empathy and theory of mind in response to emotional stimuli.


(AI) and (Ins.) stand for anterior insula and insula, respectively (z = 12 and z = 19, 15 experts and 15 novices, color codes: orange, p less than 5.10ˆ-2, yellow, p less than 2.10ˆ-2). B, C. Impulse response from rest to compassion in response to emotional sounds in AI (B) and Ins. (C). D–E. Responses in AI (D) and Ins. (E) during poor and good blocks of compassion, as verbally reported, for 12 experts (red) and 10 novices (blue).

Neuroimaging shows use of self thoughts to infer others' mental states

Jenkins et al. offer a fascinating study of how we infer the mental states of others (mentalize), making use of a phenomenon (repetition suppression) that I had not been aware of before. Here I've done a cut/paste/edit from the abstract and article to try to outline the basic idea, and also show the central figure:

One useful strategy for inferring others' mental states (i.e., mentalizing) may be to use one's own thoughts, feelings, and desires as a proxy for those of other people (This approach to social cognition is alternately described as "simulationist," "projectionist," or "self-referential".) A dorsal aspect of the medial prefrontal cortex has been associated with mentalizing about people perceived to be dissimilar from oneself, whereas a more ventral aspect of medial prefrontal cortex (vMPFC) has been linked to mentalizing about those perceived to be similar. Critically, this vMPFC region also has been observed repeatedly during tasks that require participants to introspect about their own mental experiences, suggesting a connection between tasks that require self-referential thought and those that require inferences about the mental states of similar others.

Because such techniques integrate neural activity across hundreds of thousands of neurons, activation of the same brain voxel by different tasks might occur because each activates distinct, but neighboring or interdigitated, neuronal populations. In this way, two tasks could possibly coactivate the same brain voxel despite engaging different sets of neurons that subserve disparate cognitive processes.

This technical limit can now be circumvented by recently developed paradigms that support stronger conclusions regarding the coactivation of the same neurons by different stimuli or different tasks. These techniques rely on an effect known as "repetition suppression," the observation that neural activity in stimulus-sensitive brain regions is typically reduced when a stimulus is repeated

Suppression across two stimuli indicates that the same (or at least a largely overlapping) population of neurons is engaged by both stimuli. For example, a demonstration of repetition suppression for the number "3" when it follows "4" but not when it follows "40" might suggest that a relatively high proportion of the neurons that code for the number "3" also participate in representations of similar numerosities (such as "4"), but not in representations of more distant numerosities.

If (i) repeatedly considering one's own mental states produces repetition suppression in self-sensitive regions such as vMPFC, and (ii) one engages in self-referential processing when considering the minds of similar others, then (iii) repetition suppression also should be observed when perceivers first mentalize about a similar other and then introspect about self.

Consistent with this hypothesis this perceivers spontaneously engage in self-referential processing when mentalizing about particular individuals, vMPFC response was suppressed when self-reflections followed either an initial reflection about self or a judgment of a similar, but not a dissimilar, other. These results suggest that thinking about the mind of another person may rely importantly on reference to one's own mental characteristics.

Here is the basic figure:

Figure legend (click on figure to enlarge it). A region of vMPFC (–6, 45, 3; 47 voxels in extent) was defined from an explicit self-reference task in which judgments of one's own personality characteristics were compared with judgments of another person (i.e., self > other). On a separate task, participants completed a series of paired judgments, in which they introspected about their own preferences and opinions immediately after one of three types of judgments: (i) an initial report about self (self-after-self), (ii) a judgment of a person with the same sociopolitical attitudes as oneself (self-after-similar), or (iii) a judgment of a person with opposing attitudes (self-after-dissimilar). On an equal number of trials, participants considered the identical question for prime and self or a different question across the two phases. The bar graph depicts the BOLD response associated with these self-reports after subtracting out the response associated with the initial judgment (see Methods); values therefore represent the additional BOLD response specifically associated with subsequent judgments of self. For comparison purposes, the figure includes the response in this region to self-reports made in isolation (gray bar). Significant repetition suppression was observed for self-reports that followed either an initial self-report (blue bars) or a judgment of a similar other (red bars), but not judgments of a dissimilar other (green bars). Error bars represent the 95% confidence interval for within-subject designs.

Like many of the cognitive heuristics that typically serve us well, but periodically lead to undesirable or maladaptive behavior, the use of self-reference in mentalizing may be a double-edged sword: a useful strategy for providing rich and accurate insights into the minds of similar individuals, but rife with the potential to exclude those minds assumed at first glance to be different from our own.

Moral Neuropolitics

Gary Olson, who is Chair of the Dept. of Political Science of Maravian College in Bethlehm, PA., sent me a latest draft of his article "From Mirror Neuron to Moral Neuropolitics." It does a nice job with the literature on mirror neurons and its implications, as well as political and cultural factors that enhance and inhibit moral behaviors. Gary is willing to pass on the draft article to blog readers for further comment (web version here; PDF download here).

My main comment was that the article might - in addition to covering cultural and political factors that work against moral behaviors between groups of distant people - add more data from evolutionary and developmental biology studies that also offer some evidence for factors working against morality and compassion. There is evidence for xenophobia and aggression between groups of animals (intra-group morality and cooperation, but also inter-group aggression and warfare), well documented in Chimps (cf. Feb. 19 Killer Instincts post), and other social animals (cf. March 8 post on Hyenas). Also, experiments show that that groups of children spontaneously invent not only language, but also in-groups and out-groups (cf. July 31 post) that can become competitive.