We recorded electrical activity from 532 neurons in the rostral part of inferior area 6 (area F5) of two macaque monkeys. Previous data had shown that neurons of this area discharge during goal-directed hand and mouth movements. We describe here the properties of a newly discovered set of F5 neurons ("mirror neurons', n = 92) all of which became active both when the monkey performed a given action and when it observed a similar action performed by the experimenter. Mirror neurons, in order to be visually triggered, required an interaction between the agent of the action and the object of it. The sight of the agent alone or of the object alone (three-dimensional objects, food) were ineffective. Hand and the mouth were by far the most effective agents. The actions most represented among those activating mirror neurons were grasping, manipulating and placing. In most mirror neurons (92%) there was a clear relation between the visual action they responded to and the motor response they coded. In approximately 30% of mirror neurons the congruence was very strict and the effective observed and executed actions corresponded both in terms of general action (e.g. grasping) and in terms of the way in which that action was executed (e.g. precision grip). We conclude by proposing that mirror neurons form a system for matching observation and execution of motor actions. We discuss the possible role of this system in action recognition and, given the proposed homology between F5 and human Brocca's region, we posit that a matching system, similar to that of mirror neurons exists in humans and could be involved in recognition of actions as well as phonetic gestures.

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Action recognition in the premotor cortex

The distinct modes of vision offered by feedforward and recurrent processing.

Positron emission tomography (PET) was used to identify the neural systems involved in discriminating the shape, color, and speed of a visual stimulus under conditions of selective and divided attention. Psychophysical evidence indicated that the sensitivity for discriminating subtle stimulus changes in a same-different matching task was higher when subjects selectively attended to one attribute than when they divided attention among the attributes. PET measurements of brain activity indicated that modulations of extrastriate visual activity were primarily produced by task conditions of selective attention. Attention to speed activated a region in the left inferior parietal lobule. Attention to color activated a region in the collateral sulcus and dorsolateral occipital cortex, while attention to shape activated collateral sulcus (similarly to color), fusiform and parahippocampal gyri, and temporal cortex along the superior temporal sulcus. Outside the visual system, selective and divided attention activated nonoverlapping sets of brain regions. Selective conditions activated globus pallidus, caudate nucleus, lateral orbitofrontal cortex, posterior thalamus/colliculus, and insular-premotor regions, while the divided condition activated the anterior cingulate and dorsolateral prefrontal cortex. The results in the visual system demonstrate that selective attention to different features modulates activity in distinct regions of extrastriate cortex that appear to be specialized for processing the selected feature. The disjoint pattern of activations in extravisual brain regions during selective- and divided-attention conditions also suggests that preceptual judgements involve different neural systems, depending on attentional strategies.

https://www.jneurosci.org/content/jneuro/11/8/2383.full.pdf

Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography

The functional properties of neurons located in the rostral part of inferior area 6 were studied in awake, partially restrained macaque monkeys. The most interesting property of these neurons was that their firing correlated with specific goal-related motor acts rather than with single movements made by the animal. Using the motor acts as the classification criterion we subdivided the neurons into six classes, four related to distal motor acts and two related to proximal motor acts. The distal classes are: "Grasping-with-the-hand-and-the-mouth neurons", "Grasping-with-the-hand neurons", "Holding neurons" and "Tearing neurons". The proximal classes are: "Reaching neurons" and "Bringing-to-the-mouth-or-to-the-body neurons". The vast majority of the cells belonged to the distal classes. A particularly interesting aspect of distal class neurons was that the discharge of many of them depended on the way in which the hand was shaped during the motor act. Three main groups of neurons were distinguished: "Precision grip neurons", "Finger prehension neurons", "Whole hand prehension neurons". Almost the totality of neurons fired during motor acts performed with either hand. About 50% of the recorded neurons responded to somatosensory stimuli and about 20% to visual stimuli. Visual neurons were more difficult to trigger than the corresponding neurons located in the caudal part of inferior area 6 (area F4). They required motivationally meaningful stimuli and for some of them the size of the stimulus was also critical. In the case of distal neurons there was a relationship between the type of prehension coded by the cells and the size of the stimulus effective in triggering the neurons. It is proposed that the different classes of neurons form a vocabulary of motor acts and that this vocabulary can be assessed by somatosensory and visual stimuli.

Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements.

The parieto-frontal cortical circuit that is active during action observation is the circuit with mirror properties that has been most extensively studied. Yet, there remains controversy on its role in social cognition and its contribution to understanding the actions and intentions of other individuals. Recent studies in monkeys and humans have shed light on what the parieto-frontal cortical circuit encodes and its possible functional relevance for cognition. We conclude that, although there are several mechanisms through which one can understand the behaviour of other individuals, the parieto-frontal mechanism is the only one that allows an individual to understand the action of others 'from the inside' and gives the observer a first-person grasp of the motor goals and intentions of other individuals.

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The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations.

A study has been made of the corticocortical efferent and afferent connections of the posterior bank of the arcuate sulcus in the macaque monkey. The distribution of efferent projections to the primary motor cortex (MI) was studied by injecting three different fluorescent retrograde tracers into separate regions of MI. The resultant labeling showed a discrete and topographically organized projection: neurons lying below the inferior limb of the arcuate sulcus project into the MI face area, while neurons located in the posterior bank of the inferior limb of the arcuate sulcus and in the arcuate spur region project into the MI hand area. These findings were confirmed electrophysiologically by demonstrating that postarcuate neurons could only be activated antidromically by stimulation within restricted regions of MI. HRP injections within postarcuate cortex indicated that afferents to this region arise from a number of cortical areas. However, the largest numbers of labeled neurons were found in the posterior parietal cortex (area 7b; PF) and in the secondary somatosensory region (SII). Neurons in both 7b (PF) and SII could be antidromically activated by postarcuate stimulation. It was further shown that stimulation of area 7b (PF) gives rise to short-latency synaptic responses in postarcuate neurons, including some neurons with identified projections to MI. The results are discussed in relation to the possible function of the postarcuate region of the premotor cortex in the sensory guidance of movement.

Cortical afferents and efferents of monkey postarcuate area: an anatomical and electrophysiological study.

The involvement of monkey premotor cortex neurones in preparation of visually cued arm movements.

Neuron activity was recorded in monkey cerebral cortex during a visually guided reaching task. Cells located in the banks of the arcuate sulcus at its curvature changed their activity during the period in which the monkey saw a food reward in a certain position, but before it moved to retrieve the reward. A role of these neurons in visual guidance of arm and hand movements is postulated.

M. Godschalk

Papers

Cortical afferents and efferents of monkey postarcuate area: an anatomical and electrophysiological study.

The involvement of monkey premotor cortex neurones in preparation of visually cued arm movements.

Behaviour of neurons in monkey peri-arcuate and precentral cortex before and during visually guided arm and hand movements.