Giacomo Rizzolatti

Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention

Stimuli presented in a non-attended location are responded to much slower than stimuli presented in an attended one. The hypotheses proposed to explain this effect make reference to covert movement of attention, hemifield inhibition, or attentional gradients. The experiment reported here was aimed at discriminating among these hypotheses. Subjects were cued to attend to one of four possible stimulus locations, which were arranged either horizontally or vertically, above, below, to the right or left of a fixation point. The instructions were to respond manually as fast as possible to the occurrence of a visual stimulus, regardless of whether it occurred in a cued or in a non-cued location. In 70% of the cued trials the stimulus was presented in the cued location and in 30% in one of the non-cued locations. In addition there were trials in which a non-directional cue instructed the subject to pay attention to all four locations. The results showed that the correct orienting of attention yielded a small but significant benefit; the incorrect orienting of attention yielded a large and significant cost; the cost tended to increase as a function of the distance between the attended location and the location that was actually stimulated; and an additional cost was incurred when the stimulated and attended locations were on opposite sides of the vertical or horizontal meridian. We concluded that neither the hypothesis postulating hemifield inhibition nor that postulating movement of attention with a constant time can explain the data. The hypothesis of an attention gradient and that of attention movements with a constant speed are tenable in principle, but they fail to account for the effect of crossing the horizontal and vertical meridians. A hypothesis is proposed that postulates a strict link between covert orienting of attention and programming explicit ocular movements. Attention is oriented to a given point when the oculomotor programme for moving the eyes to this point is ready to be executed. Attentional cost is the time required to erase one ocular program and prepare the next one.

Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses

The visual response of single neurons of the periarcuate cortex have been studied in the macaque monkey. Two sets of neurons responding to visual stimuli have been found. The first set, located rostral to the arcuate sulcus, was formed by units that could be activated by stimuli presented far from the animal. These neurons had large receptive fields and were neither orientation nor direction selective. The second set, found predominantly caudal to the arcuate sulcus, was formed by units that were maximally or even exclusively activated by stimuli presented in the space immediately around the animal. These neurons were bimodal, responding also to somatosensory stimuli. According to the location of their visual responding regions the bimodal neurons were subdivided into pericutaneous (54%) and distant peripersonal neurons (46%). The former responded best to stimuli presented a few centimeters from the skin, the latter to stimuli within the animals reaching distance. The visual responding regions were spatially related to the tactile fields. It is argued that neurons with a receptive field consisting of several responding areas, some in one sensory modality, some in another, have a praxic function and that they are involved in organizing sequences of movements.

Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey

The laminar pattern of cytochrome oxidase activity was studied in the agranular frontal cortex (area 4-6 complex) of the macaque monkey. The cortex, stained with this method, showed 6 stripes of different enzymatic activity. On the basis of their characteristics and of the presence of highly active cells, the agranular frontal cortex could be parcellated in 5 areas (F1-F5). F1 very likely corresponds to area FA of von Bonin and Bailey. Rostral to F1 two large regions could be distinguished, one located medial to the spur of the arcuate sulcus and its imaginary caudal extension, the other laterally. The superior region was formed by areas F2 and F3. The first was located on the dorsomedial cortical surface, the other on the mesial surface. F3 possibly corresponds to the supplementary motor area. The inferior region was formed by areas F4 and F5. The rostral area (F5) showed transition characteristics that rendered it somehow similar to the prefrontal areas. It may correspond to the cytoarchitectonic area FCBm. The cytocrome oxidase technique is a useful means of parcellating the agranular frontal cortex and may greatly help in physiological and behavioral experiments.

Hand action preparation influences the responses to hand pictures

The relations between stimuli triggering a hand grasping movement and the subsequent action were studied in normal human participants. Participants were instructed to prepare to grasp a bar, oriented either clockwise or counterclockwise, and to grasp it as fast as possible on presentation of a visual stimulus with their right hand. The visual stimuli were pictures of the right hand as seen in a mirror. In Experiment 1, they represented the mirror image of the hand final posture as achieved in grasping the bar oriented either clockwise or counterclockwise. In Experiment 2, in addition to the pictures of Experiment 1, another two pictures, obtained rotating the hands represented in the previous ones of 90 degrees, were also used. Both experiments showed that the reaction times were faster when there was a similarity between hand position as depicted in the triggering visual stimulus and the grasping hand final position, the fastest responses being those where this similarity was the closest. In addition, Experiment 2 showed that reaction times to not rotated stimuli were faster than reaction times to the rotated stimuli, thus excluding a simple stimulus-response compatibility explanation of the findings. The data are interpreted as behavioral evidence that there is a close link between specific visual stimuli and specific motor actions. A neurophysiological model for this visuo-motor link is presented.

Spatial compatibility and anatomical factors in simple and choice reaction time.

Abstract Simple reaction time to a lateralized unstructured visual stimulus was studied in subjects with hands crossed or uncrossed. Regardless of the hand position, the right hand was faster than the left hand when the stimulus was to the right of fixation, and vice versa. In both conditions there was a left visual field superiority. In a second experiment the same lateralized stimuli were presented to subjects with hands crossed or uncrossed who had to decide which hand to use depending on the position of the stimulus. In this experiment the faster hand was the one in the same visual space as the stimulus (spatial compatibility). We conclude that in simple reaction time experiments the difference between ipsilateral and contralateral reactions is due to the elementary anatomical connectivity, and that spatial compatibility becomes important only in choice situations.

Visual responses in the postarcuate cortex (area 6) of the monkey that are independent of eye position

SummaryThe visual responses of postarcuate neurons have been studied in alert behaving monkeys (Macaca nemestrina). In particular, the effect of eye position on the location of visual responses in respect to the body has been examined. It was found that a large percentage of bimodal (visual and somatosensory) neurons have visual receptive fields that are independent of eye position. The location of the visual receptive field does not change when the eyes move, but remains in register with the tactile receptive field (soma-related visually responsive neurons).

The Imitative Mind: From mirror neurons to imitation: Facts and speculations

Introduction This chapter is composed of two parts. In the first we review the functional properties of an intriguing class of premotor neurons that we discovered in the monkey premotor cortex: the “mirror neurons.” These neurons discharge both when the monkey performs an action and when it observes another individual making a similar action. The second part is basically speculative. It is based on the hypothesis that there is a very general, evolutionary ancient mechanism, that we will name “resonance” mechanism, through which pictorial descriptions of motor behaviors are matched directly on the observers motor “representations” of the same behaviors. We will posit that resonance mechanism is a fundamental mechanism at the basis of inter-individual relations including some behaviors commonly described under the heading of “imitation.” Functional properties of area F5 Motor properties Area F5 forms the rostral part of inferior area 6 (Matelli et al ., 1985). Microstimulation and single-neuron studies showed that F5 contains a hand and a mouth movement representation (Gentilucci et al ., 1988; Hepp-Reymond, Husler, Maier, & Qi, 1994; Okano & Tanji, 1987; Rizzolatti et al ., 1981; Rizzolatti et al ., 1988). Particularly interesting results were obtained when F5 neurons were studied in a semi-naturalistic context (Rizzolatti et al ., 1988). Awake monkeys were seated on a primate chair and presented with various objects (geometrical solids, pieces of food of different size and shape). The stimuli were introduced in various spatial locations around the monkey, inside and outside its peripersonal space.

Neurons related to reaching-grasping arm movements in the rostral part of area 6 (area 6aβ)

SummarySingle neurons were recorded from the rostral part of the agranular frontal cortex (area 6aβ) in awake, partially restrained macaque monkeys. In the medialmost and mesial sectors of this area, rostral to the supplementary motor area, neurons were found which were activated during arm reaching-grasping movements. These neurons (“reaching-grasping neurons”) did not appear to be influenced by how the objects were grasped nor, with some exceptions, by where they were located. Their activity changed largely prior to the arm movement and continued until the end of it. The premovement modulation (excitatory or inhibitory) could start with stimulus presentation, with the saccade triggered by the stimulus or after stimulus fixation. The distance of the stimulus from the monkey was an important variable for activating many neurons. About half of the recorded neurons showed a modulation of the same sign during movement and premovement period. The other half showed an increase/decrease in activity which was of the opposite sign during movement and premovement period or part of it. In this last case the discharge changes were of the same sign when the stimulus was close to the monkey and when the monkey moved its arm to reach the objects, whereas they were of opposite sign when the stimulus was outside the animals reach. Microstimulation of area 6aβ and the reconstruction of the locations of eye movement and arm movement related cells showed that the arm field was located more medially (and mesially) than the eye field described by Schlag and Schlag-Rey (1987). It is suggested that, unlike inferior area 6, which is mostly involved in selection of effectors on the basis of the physical properties of the objects and their spatial location (Rizzolatti and Gentilucci 1988), area 6aβ plays a role in the preparation of reaching-grasping arm movements and in their release when the appropriate conditions are set.

Movements of attention in the three spatial dimensions and the meaning of "neutral" cues.

Six experiments were conducted to examine the effect of various attentional manipulations on reaction time to visual stimuli. The first three experiments compared the responses to stimuli presented in the depth (Experiment 1), along the horizontal (Experiment 2), and vertical (Experiment 3) meridians in a valid condition (stimulus presented in the cued position), an invalid condition (stimulus presented in the alternative position to the cued position) and a neutral condition (no information on stimulus position). The most interesting result was the demonstration that attention can be moved along the sagittal plane in the absence of vergence eye movements and that when attention is focused on a certain point, unattended points between this point and the observer (i.e. near points) are responded faster than unattended points beyond it (i.e. far points). In the frontal plane no asymmetry was found between the responses to unattended points above or below the fixation, whereas a certain, albeit non-constant, advantage was present for unattended stimuli on the right of the fixation point in respect to those on the left of it. The second series of experiments was similar to the first one, except that a new situation was introduced in which the fixation point was cued and stimuli could appear either in correspondence to it or in a peripheral position (invalid condition with attention at the fixation point). The results showed that in this new situation the responses to unattended stimuli are much longer than they are under neutral conditions, and as long as they are under conventional invalid condition. It is suggested that the so called neutral condition is a condition of diffuse attention and an attempt is made to explain it in terms of a premotor theory of attention.

Action observation circuits in the macaque monkey cortex

In both monkeys and humans, the observation of actions performed by others activates cortical motor areas. An unresolved question concerns the pathways through which motor areas receive visual information describing motor acts. Using functional magnetic resonance imaging (fMRI), we mapped the macaque brain regions activated during the observation of grasping actions, focusing on the superior temporal sulcus region (STS) and the posterior parietal lobe. Monkeys viewed either videos with only the grasping hand visible or videos with the whole actor visible. Observation of both types of grasping videos activated elongated regions in the depths of both lower and upper banks of STS, as well as parietal areas PFG and anterior intraparietal (AIP). The correlation of fMRI data with connectional data showed that visual action information, encoded in the STS, is forwarded to ventral premotor cortex (F5) along two distinct functional routes. One route connects the upper bank of the STS with area PFG, which projects, in turn, to the premotor area F5c. The other connects the anterior part of the lower bank of the STS with premotor areas F5a/p via AIP. Whereas the first functional route emphasizes the agent and may relay visual information to the parieto-frontal mirror circuit involved in understanding the agents intentions, the second route emphasizes the object of the action and may aid in understanding motor acts with respect to their immediate goal.