R. Camarda

Functional organization of inferior area 6 in the macaque monkey

SummaryTwo series of experiments are reported in this paper. The first concerns the movement representation in the macaque inferior area 6, the second the functional properties of neurons located in the caudal part of this area (histochemical area F4). By combining single neuron recording and intracortical microstimulation, we found that inferior area 6 is somatotopically organized. The axio-proximal movements are represented caudally, the distal movements are represented near the arcuate sulcus. The mouth field is located laterally, the hand field medially. There is no leg field. A comparison between neuron properties and histochemical characteristics of inferior area 6 showed that the proximal movements representation includes most of area F4, whereas the distal movements representation corresponds to area F5 and to the rostral part of F4. Neurons located in that part of F4 where proximal movements are represented respond very well to tactile stimuli. They have large receptive fields mostly located on the face and on the upper part of the body. A large number of these neurons respond to visual stimuli. Objects approaching the animal are particularly effective. The tactile and the visual receptive fields are in register. The most represented movements are reaching movements, movements bringing the hand to the mouth or to the body and facial movements. There is a congruence between location of visual fields and preferred arm movements. It is argued that the receptive field arrangement and the response properties are more complex in area F4 than in the primary motor cortex and that area F4 neurons are involved in the control of arm movements towards different space sectors.

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.

Neural circuits for spatial attention and unilateral neglect

What is the relationship between attention and unilateral neglect? In this article we review three theories that have been advanced to explain this neurological syndrome, discuss their limitations, and advance an alternative hypothesis. The theories are: the hemispheric hypoarousal hypothesis (Heilman & Watson, 1977), the hypothesis of an attentional master center (see De Renzi, 1982) and the hypothesis of a cortical circuit for directing attention (Mesulam, 1981). The analysis of these theories shows that none of them is able to accomodate three basic findings: a) the multiplicity of brain centers whose lesion produces neglect; b) the congruence between attentional and motor deficits after lesion of these centers; c) the anatomical independence of centers whose damage causes neglect. A model of spatial attention is proposed based on a series of circuits largely independent one from another and formed by centers which program motor plans in a spatial framework. This conception is radically different from that of a single attentional center because it conceives spatial attention not as a supraordinate function controlling the activity of the brain as a whole, but as a property intrinsically linked to the premotor activity and distributed among various cerebral centers. In other words, spatial attention is a vertical modular function present in several independent circuits.

Visual receptive fields in the lateral suprasylvian area (Clare-Bishop area) of the cat

Single units were recorded from the visual area of the lateral suprasylvian gyrus (LSSA or Clare-Bishop area) in 20 unanesthetized cats. Most LSSA units were poorly responsive to stationary visual stimuli, but they responded vigorously to moving visual stimuli. Their receptive fields appeared to be constituted of a large activating region (discharge area) often surrounded by inhibitory flanks. Relating unit behavior to changes of stimulus length, the LSSA neurons could be subdivided into 5 categories. The first category (22 out of 95 units tested, 23.16%) consisted of units showing summation inside the discharge area. Expanding the stimulus outside the discharge area did not affect the response. The second category (7.37%) was formed by units which showed summation inside the discharge area and inhibition when the stimulus was extended outside the discharge area. The third category (21.05%) consisted of units largely insensitive to the stimulus length inside the discharge area, but surrounded by inhibitory flanks. The fourth category (41.05%) consisted of units which showed inhibition of the response when the stimulus, well inside the discharge area, became longer than a certain optimal lenght. They were surrounded by inhibitory flanks. The fifth category (7.37%) was formed by units insensitive to variations of the stimulus length inside as well as outside the discharge area. Almost all units, independent of their category, were directionally specific, that is their response could be decreased 50% or more by varying the direction of movement away from that which gave the maximal response (preferred direction). Typically the response was halved when the stimulus was moved +/- 50 degrees from the preferred direction. Among the directionally specific units, 71% showed the minimal response 180 degrees away from the preferred direction (direction specificity curve type 1), 20% had the minimal response 90 degrees from the preferred direction (direction specificity curve type 2); the remaining could not be classified in this respect. Of LSSA units, 87% (all those of type 1 and many of those of type 2) were directionally selective, that is their response to movement in the preferred direction was at least double that in the opposite direction. The LSSA units usually preferred stimuli moving at rather high speeds. The optimal speed for 71% of units was 20 degrees/sec or greater. Almost all units responded over a wide range of speeds, many of them from 5-10 degrees/sec to over 100 degrees/sec. Most neurons had a low spontaneous activity and some of them remained completely silent for seconds.

Corticospinal projections from mesial frontal and cingulate areas in the monkey

We injected neural tracers into the lateral funiculus of the spinal cord in order to relate the sites of origin of the spinal projections from the mesial cortical surface with the cytoarchitectonic organization of this region. We found a close correlation between the origin sites and density of corticospinal projections and the areal organization. The areas most densely labelled were F3 (SMA-proper) and area 24d, whereas F6 (pre-SMA) and area 24c showed a low density of labelling. The segmental topography of the corticospinal projections fitted well with the somatotopy of the mesial cortical areas. We conclude that in the agranular mesial cortex there are four independent motor representations: F3 and 24d where the whole body is represented, and F6 and 24c which are mostly related to arm movements.

Influence of the presentation of remote visual stimuli on visual responses of cat area 17 and lateral suprasylvian area.

SummarySingle units were recorded extracellularly from area 17 and lateral suprasylvian area (LSSA) in curarized cats. Visual stimuli, usually a 10 ° black spot, were introduced abruptly in the visual field remote from the discharge area of a neurons receptive field and moved at a speed of about 30 °/sec. The effect of these remote stimuli (S2) on the response to a restricted visual stimulus (S1) crossing the discharge area was studied.It was found that most units in area 17 were not affected by the presentation of remote stimuli, the remainder being either slightly facilitated or slightly inhibited. In contrast the LSSA neurons were usually inhibited by the presentation of S2: this effect was strong, was present in all classes of LSSA neurons and was independent of the relative directions of movement of S1 and S2.On the basis of these data and those previously obtained from the superior colliculus it is concluded that the way the extrageniculate centres respond to a stimulus abruptly introduced in the visual field is substantially different from that of the striate cortex. Only in the extrageniculate centres a new stimulus, besides exciting the neurons which correspond to the position of the stimulus in the field, concomitantly decreases the responses of neurons located in positions of the visual field remote from that stimulus. Possible behavioral implications of the findings are discussed.

Interconnections within the postarcuate cortex (area 6) of the macaque monkey.

Small amounts of horseradish peroxidase conjugated with wheat germ were injected in restricted parts of the postarcuate premotor area of the macaque monkey. It was found that regions of this area having different somatotopic representations are richly interconnected among them. This pattern of intra-areal connectivity was not observed in the precentral motor area. It appears therefore that the postarcuate area is organized according to anatomical principles which are different from those of the primary motor cortex.

Somatotopic Representation in Inferior Area 6 of the Macaque Monkey

On the basis of its cytoarchitectonic and enzymatic properties area 6 of the macaque monkey can be subdivided into two large sectors: a superior sector lying medial to the spur of the arcuate sulcus (superior area 6 or F2) and an inferior sector lying lateral to it (inferior area 6). Inferior area 6 is constituted by two enzymatic areas: F4 and F5. In this study we investigated the somatotopic organization of inferior area 6 and the adjacent area 4 combining single-neuron recording and intracortical electrical microstimulation. We found that two separate movement representations exist in this region. The caudal one corresponds to area F1 (primary motor cortex), the rostral one to inferior area 6. The two representations are mirror images one of the other with the axioproximal movements being adjacently located. In the rostral map the proximal movements are mostly located in F4, the distal movements in F5. Neuronal properties indicate that the rostral map has characteristics that are more complex than the caudal map. We propose that the rostral map is involved in transforming visual information in motor commands. F4 should be involved in the control of arm movements based on the location of the objects in respect to the body, whereas F5 should play a role in the control of grasping movements on the basis of the size of the stimuli.

Neurons with complex visual properties in the superior colliculus of the macaque monkey

SummarySingle neurons were recorded from the superficial layers of the superior colliculus of immobilized monkeys (Macaca mulatta and Macaca irus). Two main functional types of neurons were found. The neurons of the first type (Type I neurons) responded well to simple stationary and moving stimuli such as spots, bars or slits of light. The latency of their response was 41 ± 6 ms. They were not directionally selective and responded to a large range of velocities.The neurons of the second type (Type II neurons) responded very poorly to simple visual stimuli and their activation required real objects or certain two-dimensional patterns. The mean latency of response of these units was 66 ± 26 ms. Habituation was always present. Type II neurons were located in the lower part of the superficial layers.The characteristics of Type II neurons suggest that in the primate superior colliculus there is a mechanism that allows the recognition of the complexity and the novelty of a stimulus and guides orienting responses to those stimuli that are worth analyzing in detail.

Units of monkey superior colliculus responding to complex visual stimuli

Single-unit activity was recorded in the superior colliculus of awake curarized monkeys (Macaca irus). In addition to movement-sensitive, non-directionally selective units 1,2,3, we have found other units which were poorly or not at all triggered by the traditional light and dark two-dimensional stimuli, but which responded vigorously to the presentation of complex moving or stationary stimuli (especially three-dimensional objects) ~. The responses were not specific to a particular object, but some objects were more effective than others. Gradual habituation of the response after repeated presentation of the object was always found, but subsequent presentation of a new object in the receptive field produced a brisk response and in some units dishabituated the response to the old stimulus. Extrafield presentation of a new stimulus never had this effect, nor was there habituation to objects presented repeatedly outside the receptive field and then within the receptive field. This last finding makes it very unlikely that the effects are related to general arousal. These results suggest that units in the superior colliculus of the monkey are capable of distinguishing between different objects and that their firing rate reflects the newness of the stimulus. Further experiments are in progress to clarify the importance of cortico-collicular pathways in determining this discriminative capacity.