Dylan F. Cooke

Parieto-frontal interactions, personal space, and defensive behavior.

In the monkey brain, two interconnected cortical areas have distinctive neuronal responses to visual, tactile, and auditory stimuli. These areas are the ventral intraparietal area (VIP) and a polysensory zone in the precentral gyrus (PZ). The multimodal neurons in these areas typically respond to objects touching, near, or looming toward the body surface. Electrical stimulation of these areas evokes defensive-like withdrawing or blocking movements. These areas have been suggested to participate in a range of functions including navigation by optic flow, attention to nearby space, and the processing of object location for the guidance of movement. We suggest that a major emphasis of these areas is the construction of a margin of safety around the body and the selection and coordination of defensive behavior. In this review, we summarize the physiological properties of these brain areas and discuss a range of behavioral phenomena that might be served by those neuronal properties, including the ducking and blocking reactions that follow startle, the flight zone of animals, the personal space of humans, the nearby, multimodal attentional space that has been studied in humans, the withdrawal reaction to looming visual stimuli, and the avoidance of obstacles during self-motion such as locomotion or reaching.

The cortical control of movement revisited

Recently, we found that electrical stimulation of motor cortex caused monkeys to make coordinated, complex movements. These evoked movements were arranged across the cortex in a map of spatial locations to which the hand moved. We suggest that some of the subdivisions previously described within primary motor and premotor cortex may represent different types of actions that monkeys tend to make in different regions of space. According to this view, primary and premotor cortex may fit together into a larger map of manual space.

Complex movements evoked by microstimulation of the ventral intraparietal area

Most neurons in the ventral intraparietal area (VIP) of the macaque brain respond to both visual and tactile stimuli. The tactile receptive field is usually on the face, and the visual receptive field usually corresponds spatially to the tactile receptive field. In this study, electrical microstimulation of VIP, but not of surrounding tissue, caused a constellation of movements including eye closure, facial grimacing, head withdrawal, elevation of the shoulder, and movements of the hand to the space beside the head or shoulder. A similar set of movements was evoked by an air puff to the monkeys cheek. One interpretation is that VIP contributes to defensive movements triggered by stimuli on or near the head.

Parallel Evolution of Cortical Areas Involved in Skilled Hand Use

Dexterous hands, used to manipulate food, tools, and other objects, are one of the hallmarks of primate evolution. However, the neural substrate of fine manual control necessary for these behaviors remains unclear. Here, we describe the functional organization of parietal cortical areas 2 and 5 in the cebus monkey. Whereas other New World monkeys can be quite dexterous, and possess a poorly developed area 5, cebus monkeys are the only New World primate known to use a precision grip, and thus have an extended repertoire of manual behaviors. Unlike other New World Monkeys, but much like the macaque monkey, cebus monkeys possess a proprioceptive cortical area 2 and a well developed area 5, which is associated with motor planning and the generation of internal body coordinates necessary for visually guided reaching, grasping, and manipulation. The similarity of these fields in cebus monkeys and distantly related macaque monkeys with similar manual abilities indicates that the range of cortical organizations that can emerge in primates is constrained, and those that emerge are the result of highly conserved developmental mechanisms that shape the boundaries and topographic organizations of cortical areas.

All Rodents Are Not the Same: A Modern Synthesis of Cortical Organization

Rodents are a major order of mammals that is highly diverse in distribution and lifestyle. Five suborders, 34 families, and 2,277 species within this order occupy a number of different niches and vary along several lifestyle dimensions such as diel pattern (diurnal vs. nocturnal), terrain niche, and diet. For example, the terrain niche of rodents includes arboreal, aerial, terrestrial, semi-aquatic, burrowing, and rock dwelling. Not surprisingly, the behaviors associated with particular lifestyles are also highly variable and thus the neocortex, which generates these behaviors, has undergone corresponding alterations across species. Studies of cortical organization in species that vary along several dimensions such as terrain niche, diel pattern, and rearing conditions demonstrate that the size and number of cortical fields can be highly variable within this order. The internal organization of a cortical field also reflects lifestyle differences between species and exaggerates behaviorally relevant effectors such as vibrissae, teeth, or lips. Finally, at a cellular level, neuronal number and density varies for the same cortical field in different species and is even different for the same species reared in different conditions (laboratory vs. wild-caught). These very large differences across and within rodent species indicate that there is no generic rodent model. Rather, there are rodent models suited for specific questions regarding the development, function, and evolution of the neocortex.

Super-flinchers and nerves of steel: Defensive movements altered by chemical manipulation of a cortical motor area

In a restricted zone of the monkey motor cortex, neurons respond to objects near, approaching, or touching the body. This polysensory zone was hypothesized to play a role in monitoring nearby stimuli for the guidance of defensive movements. To test this hypothesis, we chemically manipulated sites within that zone by injecting bicuculline (increasing neuronal activity) or muscimol (decreasing neuronal activity). Bicuculline caused the monkey to react in an exaggerated fashion to an air puff on the face and to objects approaching the face, whereas muscimol caused the monkey to react in a reduced fashion. The effects were expressed partly as a motor abnormality (affecting movement of the musculature contralateral to the injection site) but also partly as a sensory enhancement or sensory neglect (affecting responses to stimuli contralateral to the injection site). These findings suggest that the polysensory zone contributes to the ethologically important function of defense of the body.

Distribution of hand location in monkeys during spontaneous behavior

Recently it was shown that electrical stimulation of the precentral gyrus of monkeys can evoke complex, coordinated movements. In the forelimb representation, stimulation of each site caused the arm to move to a specific final posture, and thus the hand to move to a location in space. Among these stimulation-evoked hand locations, certain regions of the hand’s workspace were more represented than others. We hypothesized that a similar non-uniform distribution of hand location should be present during a monkey’s spontaneous behavior. The present study examined the distribution of hand location of monkeys in their home cages. This distribution was similar to that found by stimulation of the precentral gyrus. That is, arm postures that were over-represented in spontaneous behavior were also over-represented in the movements evoked by cortical stimulation.

Lesions in Posterior Parietal Area 5 in Monkeys Result in Rapid Behavioral and Cortical Plasticity

We examined the effects of focal lesions of posterior parietal area 5 in macaque monkeys on bimanual behavior performed with and without visual guidance. The animals were trained on two reaching tasks and one tactile texture discrimination task. Task 1 simply involved reaching toward and grasping a reward from one of five well positions. Task 2 required the monkey to use both hands simultaneously to obtain a reward. The tactile texture discrimination task required the monkey to signal the roughness of a passively delivered texture using its jaw. After lesions to area 5, the monkeys showed a decrease in hand use for tasks 1 and 2 and an inability to perform task 2 in specific locations in visual space. These deficits recovered within several days. No deficits were observed in the tactile texture discrimination task or in an analgesic control monkey. Electrophysiological recordings made just before the lesion, immediately after the lesion, and 2 months after the lesion demonstrated that cortical areas just rostral to the lesioned area 5, and areas 1 and 2, were topographically reorganized and that receptive fields for neurons in these fields changed location on the body surface. These cortical map changes are correlative and may, in part, contribute to the rapid behavioral recovery observed. The mechanism for such rapid changes may be the unmasking of existing divergent and convergent thalamocortical connections that are part of the normal cortical circuitry.

Reversible deactivation of higher-order posterior parietal areas. I. Alterations of receptive field characteristics in early stages of neocortical processing

Somatosensory processing in the anesthetized macaque monkey was examined by reversibly deactivating posterior parietal areas 5L and 7b and motor/premotor cortex (M1/PM) with microfluidic thermal regulators developed by our laboratories. We examined changes in receptive field size and configuration for neurons in areas 1 and 2 that occurred during and after cooling deactivation. Together the deactivated fields and areas 1 and 2 form part of a network for reaching and grasping in human and nonhuman primates. Cooling area 7b had a dramatic effect on receptive field size for neurons in areas 1 and 2, while cooling area 5 had moderate effects and cooling M1/PM had little effect. Specifically, cooling discrete locations in 7b resulted in expansions of the receptive fields for neurons in areas 1 and 2 that were greater in magnitude and occurred in a higher proportion of sites than similar changes evoked by cooling the other fields. At some sites, the neural receptive field returned to the precooling configuration within 5-22 min of rewarming, but at other sites changes in receptive fields persisted. These results indicate that there are profound top-down influences on sensory processing of early cortical areas in the somatosensory cortex.

Intracortical Microstimulation Maps of Motor, Somatosensory, and Posterior Parietal Cortex in Tree Shrews (Tupaia belangeri) Reveal Complex Movement Representations

Abstract Long‐train intracortical microstimulation (LT‐ICMS) is a popular method for studying the organization of motor and posterior parietal cortex (PPC) in mammals. In primates, LT‐ICMS evokes both multijoint and multiple‐body‐part movements in primary motor, premotor, and PPC. In rodents, LT‐ICMS evokes complex movements of a single limb in motor cortex. Unfortunately, very little is known about motor/PPC organization in other mammals. Tree shrews are closely related to both primates and rodents and could provide insights into the evolution of complex movement domains in primates. The present study investigated the extent of cortex in which movements could be evoked with ICMS and the characteristics of movements elicited using both short train (ST) and LT‐ICMS in tree shrews. We demonstrate that LT‐ICMS and ST‐ICMS maps are similar, with the movements elicited with ST‐ICMS being truncated versions of those elicited with LT‐ICMS. In addition, LT‐ICMS‐evoked complex movements within motor cortex similar to those in rodents. More complex movements involving multiple body parts such as the hand and mouth were also elicited in motor cortex and PPC, as in primates. Our results suggest that complex movement networks present in PPC and motor cortex were present in mammals prior to the emergence of primates.