Perceptual inference

Perceptual inference refers to the ability to infer sensory stimuli from predictions that result from internal neural representations built through prior experience. Methods of Bayesian statistical inference and decision theory model cognition adequately by using error sensing either in guiding action or in “generative” models that predict the sensory information. In this framework, perception can be seen as a process qualitatively distinct from sensation, a process of information evaluation using previously acquired and stored representations (memories) that is guided by sensory feedback. The stored representations can be utilised as internal models of sensory stimuli enabling long term associations, for example in operant conditioning. Evidence for perceptual inference is contributed by such phenomena as the cortical co-localisation of object perception with object memory, the response invariance in the responses of some neurons to variations in the stimulus, as well as from situations in which perception can be dissociated from sensation. In the context of perceptual inference, sensory areas of the cerebral cortex that have been facilitated by a priming signal may be regarded as comparators in a closed feedback loop, similar to the better known motor reflexes in the sensorimotor system. The adult cerebral cortex can be regarded as similar to a servomechanism, in using sensory feedback to correct internal models, producing predictions of the outside world on the basis of past experience.     

More than an imitation game: Top-down modulation of the human mirror system

All interpersonal interactions are underpinned by action: perceiving and understanding the actions of others, and responding by planning and performing self-made actions. Perception of action, both self-made and observed, informs ongoing motor responses by iterative feedback within a perception-action loop. This fundamental phenomenon occurs within single-cells of the macaque brain which demonstrate sensory and motor response properties. These ‘mirror’ neurons have led to a swathe of research leading to the broadly accepted idea of a human mirror system. The current review examines the putative human mirror system literature to highlight several inconsistencies in comparison to the seminal macaque data, and ongoing controversies within human focused research (including mirror neuron origin and function). In particular, we will address the often-neglected other side to the ‘mirror’: complementary and opposing actions. We propose that engagement of the mirror system in meeting changing task-demands is dynamically modulated via frontal control networks.     

Les neurones miroirs

The neurophysiological studies of the last two decades have provided evidence that the motor cortex is not simply involved in movement programming and execution, but plays a main role in coding the goal of motor acts. The presence of dedicated anatomical circuits linking single premotor areas with specific areas of the posterior parietal cortex allows motor representations to be matched with several types of sensory inputs, thus allowing several types of sensorimotor integrations. An example of this matching mechanism is represented by mirror neurons, found in both the ventral premotor and the inferior parietal cortex of the monkey, responding during both observation and execution of hand and mouth motor acts. This capacity would allow individuals to understand the meaning of motor acts done by others. More recent studies on the response of these neurons during observation of motor acts performed at different distances suggested that they could play a role also in triggering different types of behavioral reactions. Furthermore, other recent studies indicate that mirror neurons may also have an important role in decoding the motor intention of others. A bulk of studies showed the presence of a parieto-premotor mirror system also in humans. Interestingly, some human studies demonstrated that this system could be modified by motor experience. This plasticity has been exploited in motor rehabilitation, to assess whether stroke patients can improve their motor function after an observation therapy. The results are positive and it seems that this therapy can be employed successfully also in children with cerebral palsy.     

Mirror neurons and motor intentionality

Our social life rests to a large extent on our ability to understand the intentions of others. What are the bases of this ability? A very influential view is that we understand the intentions of others because we are able to represent them as having mental states. Without this meta-representational (mind-reading) ability their behavior would be meaningless to us. Over the past few years this view has been challenged by neurophysiological findings and, in particular, by the discovery of mirror neurons. The functional properties of these neurons indicate that intentional understanding is based primarily on a mechanism that directly matches the sensory representation of the observed actions with one's own motor representation of those same actions. These findings reveal how deeply motor and intentional components of action are intertwined, suggesting that both can be fully comprehended only starting from a motor approach to intentionality.     

Feedback in the brainstem: An excitatory disynaptic pathway for control of whisking

Sensorimotor processing relies on hierarchical neuronal circuits to mediate sensory‐driven behaviors. In the mouse vibrissa system, trigeminal brainstem circuits are thought to mediate the first stage of vibrissa scanning control via sensory feedback that provides reflexive protraction in response to stimulation. However, these circuits are not well defined. Here we describe a complete disynaptic sensory receptor‐to‐muscle circuit for positive feedback in vibrissa movement. We identified a novel region of trigeminal brainstem, spinal trigeminal nucleus pars muralis, which contains a class of vGluT2+ excitatory projection neurons involved in vibrissa motor control. Complementary single‐ and dual‐labeling with traditional and virus tracers demonstrate that these neurons both receive primary inputs from vibrissa sensory afferent fibers and send monosynaptic connections to facial nucleus motoneurons that directly innervate vibrissa musculature. These anatomical results suggest a general role of disynaptic architecture in fast positive feedback for motor output that drives active sensation. J. Comp. Neurol. 523:921–942, 2015. © 2014 Wiley Periodicals, Inc.     

Just seeing you makes me feel better: Interpersonal enhancement of touch

Abstract

The human brain may contain “mirror systems” allowing mental simulation of the sensorimotor states of others. Most research has focused on interpersonal sharing of motor representations, with relatively little focus on sensation. Here we show that viewing the body of another person significantly enhances the spatial resolution of touch on the corresponding body part. Thirty subjects judged the orientation of gratings presented to the index finger tip, either when viewing their own hand, when viewing a neutral object presented in approximately the same location, or when viewing the undisguised hand of a third person standing behind them. Orientation discrimination was significantly more accurate when viewing one's own body compared to when viewing a neutral object. The same enhancement effect was found when viewing another's body. Performance when viewing one's own body did not differ significantly from performance when viewing the body of another person. This result suggests a purely sensory interpersonal sharing of body representations. It also suggests a specifically interpersonal modulation of primary sensory functions within the brain.     

Just seeing you makes me feel better: interpersonal enhancement of touch

The human brain may contain "mirror systems" allowing mental simulation of the sensorimotor states of others. Most research has focused on interpersonal sharing of motor representations, with relatively little focus on sensation. Here we show that viewing the body of another person significantly enhances the spatial resolution of touch on the corresponding body part. Thirty subjects judged the orientation of gratings presented to the index finger tip, either when viewing their own hand, when viewing a neutral object presented in approximately the same location, or when viewing the undisguised hand of a third person standing behind them. Orientation discrimination was significantly more accurate when viewing one's own body compared to when viewing a neutral object. The same enhancement effect was found when viewing another's body. Performance when viewing one's own body did not differ significantly from performance when viewing the body of another person. This result suggests a purely sensory interpersonal sharing of body representations. It also suggests a specifically interpersonal modulation of primary sensory functions within the brain.     

Sensorimotor cortex as a critical component of an 'extended' mirror neuron system: Does it solve the development,correspondence, and control problems in mirroring?

A core assumption of how humans understand and infer the intentions and beliefs of others is the existence of a functional self-other distinction. At least two neural systems have been proposed to manage such a critical distinction. One system, part of the classic motor system, is specialized for the preparation and execution of motor actions that are self realized and voluntary, while the other appears primarily involved in capturing and understanding the actions of non-self or others. The latter system, of which the mirror neuron system is part, is the canonical action 'resonance' system in the brain that has evolved to share many of the same circuits involved in motor control. Mirroring or 'shared circuit systems' are assumed to be involved in resonating, imitating, and/or simulating the actions of others. A number of researchers have proposed that shared representations of motor actions may form a foundational cornerstone for higher order social processes, such as motor learning, action understanding, imitation, perspective taking, understanding facial emotions, and empathy. However, mirroring systems that evolve from the classic motor system present at least three problems: a development, a correspondence, and a control problem. Developmentally, the question is how does a mirroring system arise? How do humans acquire the ability to simulate through mapping observed onto executed actions? Are mirror neurons innate and therefore genetically programmed? To what extent is learning necessary? In terms of the correspondence problem, the question is how does the observer agent know what the observed agent's resonance activation pattern is? How does the matching of motor activation patterns occur? Finally, in terms of the control problem, the issue is how to efficiently control a mirroring system when it is turned on automatically through observation? Or, as others have stated the problem more succinctly: "Why don't we imitate all the time?" In this review, we argue from an anatomical, physiological, modeling, and functional perspectives that a critical component of the human mirror neuron system is sensorimotor cortex. Not only are sensorimotor transformations necessary for computing the patterns of muscle activation and kinematics during action observation but they provide potential answers to the development, correspondence and control problems.     

Controlling the alien hand through the mirror box. A single case study of Alien Hand Syndrome

Disruption of motor control in the alien hand syndrome might result from a dissociation between intentions and sensory information. We hypothesized that voluntary motor control in this condition could improve by restoring the congruency between motor intentions and visual feedback. The present study shows that, in one patient with right alien hand syndrome, the use of a mirror box paradigm improved motor speed. We speculate that the visual feedback provided by the mirror increases the sense of congruence between intention and sensory feedback, leading to motor improvement.     

Neurones miroirs,substrat neuronal de la compréhension de l’action?

In 1992, the Laboratory of Human Physiology at the University of Parma (Italy) publish a study describing “mirror” neurons in the macaque that activate both when the monkey performs an action and when it observes an experimenter performing the same action. The research team behind this discovery postulates that the mirror neurons system is the neural basis of our ability to understand the actions of others, through the motor mapping of the observed action on the observer's motor repertory (direct-matching hypothesis). Nevertheless, this conception met serious criticism. These critics attempt to relativize their function by placing them within a network of neurocognitive and sensory interdependencies. In short, the essential characteristic of these neurons is to combine the processing of sensory information, especially visual, with that of motor information. Their elementary function would be to provide a motor simulation of the observed action, based on visual information from it. They can contribute, with other non-mirror areas, to the identification/prediction of the action goal and to the interpretation of the intention of the actor performing it. Studying the connectivity and high frequency synchronizations of the different brain areas involved in action observation would likely provide important information about the dynamic contribution of mirror neurons to “action understanding”. The aim of this review is to provide an up-to-date analysis of the scientific evidence related to mirror neurons and their elementary functions, as well as to shed light on the contribution of these neurons to our ability to interpret and understand others’ actions.     

Interpreting actions: the goal behind mirror neuron function

Crucial to our everyday social functioning is an ability to interpret the behaviors of others. This process involves a rapid understanding of what a given action is not only in a physical sense (e.g., a precision grip around the stem of a wine glass) but also in a semantic sense (e.g., an invitation to "cheers"). The functional properties of fronto-parietal mirror neurons (MNs), which respond to both observed and executed actions, have been a topic of much debate in the cognitive neuroscience literature. The controversy surrounds the role of the "mirror neuron system" in action understanding: do MNs allow us to comprehend others' actions by allowing us to internally represent their behaviors or do they simply activate a direct motor representation of the perceived act without recourse to its meaning? This review outlines evidence from both human and primate literatures, indicating the importance of end-goals in action representations within the motor system and their predominance in influencing action plans. We integrate this evidence with recent views regarding the complex and dynamic nature of the mirror neuron system and its ability to respond to broad motor outcomes.     

Mirror neurons responding to observation of actions made with tools in monkey ventral premotor cortex

In the present study, we describe a new type of visuomotor neurons, named tool-responding mirror neurons, which are found in the lateral sector of monkey ventral premotor area F5. Tool-responding mirror neurons discharge when the monkey observes actions performed by an experimenter with a tool (a stick or a pair of pliers). This response is stronger than that obtained when the monkey observes a similar action made with a biological effector (the hand or the mouth). These neurons respond also when the monkey executes actions with both the hand and the mouth. The visual and the motor responses of each neuron are congruent in that they share the same general goal, that is, taking possession of an object and modifying its state. It is hypothesized that after a relatively long visual exposure to tool actions, a visual association between the hand and the tool is created, so that the tool becomes as a kind of prolongation of the hand. We propose that tool-responding mirror neurons enable the observing monkey to extend action-understanding capacity to actions that do not strictly correspond to its motor representations. Our findings support the notion that the motor cortex plays a crucial role in understanding action goals.     

Rapid and persistent impairments of the forelimb motor representations following cervical deafferentation in rats

Skilled motor control is regulated by the convergence of somatic sensory and motor signals in brain and spinal motor circuits. Cervical deafferentation is known to diminish forelimb somatic sensory representations rapidly and to impair forelimb movements. Our focus was to determine what effect deafferentation has on the motor representations in motor cortex, knowledge of which could provide new insights into the locus of impairment following somatic sensory loss, such as after spinal cord injury or stroke. We hypothesized that somatic sensory information is important for cortical motor map topography. To investigate this we unilaterally transected the dorsal rootlets in adult rats from C4 to C8 and mapped the forelimb motor representations using intracortical microstimulation, immediately after rhizotomy and following a 2‐week recovery period. Immediately after deafferentation we found that the size of the distal representation was reduced. However, despite this loss of input there were no changes in motor threshold. Two weeks after deafferentation, animals showed a further distal representation reduction, an expansion of the elbow representation, and a small elevation in distal movement threshold. These changes were specific to the forelimb map in the hemisphere contralateral to deafferentation; there were no changes in the hindlimb or intact‐side forelimb representations. Degradation of the contralateral distal forelimb representation probably contributes to the motor control deficits after deafferentation. We propose that somatic sensory inputs are essential for the maintenance of the forelimb motor map in motor cortex and should be considered when rehabilitating patients with peripheral or spinal cord injuries or after stroke.     

Towards a common neural substrate in the immediate and effective inhibition of stuttering

Stuttering can be effectively inhibited via exogenous sensory signals (e.g., speaking in unison or using altered auditory feedback) or by using endogenous motoric strategies (e.g., singing or therapeutically implementing long vowel prolongations to reduce speech rates). We propose that these channels, which superficially appear to be diametrically opposite, centrally converge in the engagement of mirror neurons for fluent gestural productions. Sensory changes incurred via exogenous speech signals allow for direct engagement of mirror systems, while endogenous motor strategies appear to require significant departures from normal speech production (e.g., highly unnatural or droned speech) to engage mirror systems. Thus, paradoxically, stuttering is prone to resurface during attempts to impose naturalness upon therapeutic speech.     

TOWARDS A COMMON NEURAL SUBSTRATE IN THE IMMEDIATE AND EFFECTIVE INHIBITION OF STUTTERING

Stuttering can be effectively inhibited via exogenous sensory signals (e.g., speaking in unison or using altered auditory feedback) or by using endogenous motoric strategies (e.g., singing or therapeutically implementing long vowel prolongations to reduce speech rates). We propose that these channels, which superficially appear to be diametrically opposite, centrally converge in the engagement of mirror neurons for fluent gestural productions. Sensory changes incurred via exogenous speech signals allow for direct engagement of mirror systems, while endogenous motor strategies appear to require significant departures from normal speech production (e.g., highly unnatural or droned speech) to engage mirror systems. Thus, paradoxically, stuttering is prone to resurface during attempts to impose naturalness upon therapeutic speech     

Functional organization of inferior parietal lobule convexity in the macaque monkey: electrophysiological characterization of motor, sensory and mirror responses and their correlation with cytoarchitectonic areas

The general view on the functional role of the monkey inferior parietal lobule (IPL) convexity mainly derives from studies carried out more than two decades ago and does not account for the functional complexity suggested by more recent neuroanatomical findings. We investigated this issue by recording multi- and single units in the IPL convexity of two monkeys and characterizing their somatosensory, visual and motor responses, using a naturalistic (ethologically relevant) approach. These properties were then matched with IPL cytoarchitectonic parcellation. A further aim of this study was to describe the general properties and the localization of IPL mirror neurons, until now not investigated in detail. Results showed that each studied cytoarchitectonic subdivision of the IPL (PF, PFG, PG) is characterized by specific sensory and motor properties. A key feature of the recorded motor neurons is that of coding goal-directed motor acts. Motor responses are somatotopically organized in a rostro-caudal fashion, with mouth, hand and arm represented in PF, PFG and PG, respectively, with a certain degree of overlap between adjacent representations. In each subdivision the motor activity is associated with specific somatosensory and visual responses, suggesting that each area organizes motor acts in different space sectors. Mirror neurons have been found mainly in area PFG and their general features appear to be very similar to those of ventral premotor mirror neurons. The present data suggest that the IPL plays an important role in both action organization and action understanding and should be considered part of the motor system.     

Action observation and execution: what is shared?

Performing an action and observing it activate the same internal representations of action. The representations are therefore shared between self and other (shared representations of action, SRA). But what exactly is shared? At what level within the hierarchical structure of the motor system do SRA occur? Understanding the content of SRA is important in order to decide what theoretical work SRA can perform. In this paper, we provide some conceptual clarification by raising three main questions: (i) are SRA semantic or pragmatic representations of action?; (ii) are SRA sensory or motor representations?; (iii) are SRA representations of the action as a global unit or as a set of elementary motor components? After outlining a model of the motor hierarchy, we conclude that the best candidate for SRA is intentions in action, defined as the motor plans of the dynamic sequence of movements. We shed new light on SRA by highlighting the causal efficacy of intentions in action. This in turn explains phenomena such as inhibition of imitation.     

The Errors of Our Ways: Understanding Error Representations in Cerebellar-Dependent Motor Learning

The cerebellum is essential for error-driven motor learning and is strongly implicated in detecting and correcting for motor errors. Therefore, elucidating how motor errors are represented in the cerebellum is essential in understanding cerebellar function, in general, and its role in motor learning, in particular. This review examines how motor errors are encoded in the cerebellar cortex in the context of a forward internal model that generates predictions about the upcoming movement and drives learning and adaptation. In this framework, sensory prediction errors, defined as the discrepancy between the predicted consequences of motor commands and the sensory feedback, are crucial for both on-line movement control and motor learning. While many studies support the dominant view that motor errors are encoded in the complex spike discharge of Purkinje cells, others have failed to relate complex spike activity with errors. Given these limitations, we review recent findings in the monkey showing that complex spike modulation is not necessarily required for motor learning or for simple spike adaptation. Also, new results demonstrate that the simple spike discharge provides continuous error signals that both lead and lag the actual movements in time, suggesting errors are encoded as both an internal prediction of motor commands and the actual sensory feedback. These dual error representations have opposing effects on simple spike discharge, consistent with the signals needed to generate sensory prediction errors used to update a forward internal model.     

Motor cortex stimulation in patients with post-stroke pain: conscious somatosensory response and pain control

We analyzed the conscious sensory responses to cortical stimulation of 31 patients with post-stroke pain who underwent motor cortex stimulation (MCS) therapy. During surgery for electrode placement, a sensory response (tingle projected to a localized peripheral area) was elicited by high-frequency stimulation (50 Hz) in 23 (84%) from the somatosensory cortex, and in 16 (52%) from the motor cortex without muscle contraction. Unpleasant painful sensation was induced or their original pain was exacerbated in 12 patients (39%) when the somatosensory cortex was stimulated and in two (6%) when the motor cortex was stimulated. Somatosensory responses were induced in eight (25%) even by low-frequency stimulation (1-2 Hz) of the motor cortex at an intensity below the threshold for muscle contraction. In contrast, among 20 nonpain patients who underwent a similar procedure for cortical mapping in epilepsy or brain tumor surgery, a sensory response was produced by high-frequency stimulation in only eight (40%; p < 0.02) from the somatosensory cortex and four (20%; p < 0.03) from the motor cortex. Pain sensation was not induced by stimulation of the somatosensory cortex (p < 0.002) or motor cortex in any of these patients. In addition, none of these patients reported a sensory response to low-frequency stimulation. In both of the two post-stroke pain patients who reported abnormal pain sensation in response to stimulation of the motor cortex, MCS failed to control their post-stroke pain. These findings imply that the sensitivity of the perceptual system even to activity of the motor cortex is heightened in post-stroke pain patients, which can sometimes hinder pain control by MCS.