Jeffrey Padberg

Cortical connections of the second somatosensory area and the parietal ventral area in macaque monkeys

To gain insight into how cortical fields process somatic inputs and ultimately contribute to complex abilities such as tactile object perception, we examined the pattern of connections of two areas in the lateral sulcus of macaque monkeys: the second somatosensory area (S2), and the parietal ventral area (PV). Neuroanatomical tracers were injected into electrophysiologically and/or architectonically defined locations, and labeled cell bodies were identified in cortex ipsilateral and contralateral to the injection site. Transported tracer was related to architectonically defined boundaries so that the full complement of connections of S2 and PV could be appreciated. Our results indicate that S2 is densely interconnected with the primary somatosensory area (3b), PV, and area 7b of the ipsilateral hemisphere, and with S2, 7b, and 3b in the opposite hemisphere. PV is interconnected with areas 3b and 7b, with the parietal rostroventral area, premotor cortex, posterior parietal cortex, and with the medial auditory belt areas. Contralateral connections were restricted to PV in the opposite hemisphere. These data indicate that S2 and PV have unique and overlapping patterns of connections, and that they comprise part of a network that processes both cutaneous and proprioceptive inputs necessary for tactile discrimination and recognition. Although more data are needed, these patterns of interconnections of cortical fields and thalamic nuclei suggest that the somatosensory system may not be segregated into two separate streams of information processing, as has been hypothesized for the visual system. Rather, some fields may be involved in a variety of functions that require motor and sensory integration. J. Comp. Neurol. 462:382–399, 2003.

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.

Topographic Maps within Brodmann's Area 5 of Macaque Monkeys

Brodmanns area 5 has traditionally included the rostral bank of the intraparietal sulcus (IPS) as well as posterior portions of the postcentral gyrus and medial wall. However, different portions of this large architectonic zone may serve different functions related to reaching and grasping behaviors. The current study used multiunit recording techniques in anesthetized macaque monkeys to survey a large extent of the rostral bank of the IPS so that hundreds of recording sites could be used to determine the functional subdivisions and topographic organization of cortical areas in this region. We identified a lateral area on the rostral IPS that we term area 5L. Area 5L contains neurons with receptive fields on mostly the shoulder, forelimb, and digits, with no apparent representation of other body parts. Thus, there is a large magnification of the forelimb. Receptive fields for neurons in this region often contain multiple joints of the forelimb or multiple digits, which results in imprecise topography or fractures in map organization. Our results provide the first overall topographic map of area 5L obtained in individual macaque monkeys and suggest that this region is distinct from more medial portions of the IPS.

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.

Thalamocortical connections of anterior and posterior parietal cortical areas in New World titi monkeys.

We examined the thalamocortical connections of electrophysiologically identified locations in the hand and forelimb representations in areas 3b, 1, and 5 in the New World titi monkeys (Callicebus moloch), and of area 7b/AIP. Labeled cells and terminals in the thalamus resulting from the injections were related to architectonic boundaries. As in previous studies in primates, the hand representation of area 3b has dense, restricted projections predominantly from the lateral division of the ventral posterior nucleus (VPl). Projections to area 1 were highly convergent from several thalamic nuclei including the ventral lateral nucleus (VL), anterior pulvinar (PA), VPl, and the superior division of the ventral posterior nucleus (VPs). In cortex immediately caudal to area 1, what we term area 5, thalamocortical connections were also highly convergent and predominantly from nuclei of the thalamus associated with motor, visual, or somatic processing such as VL, the medial pulvinar (PM), and PA, respectively; with moderate projections from VP, central lateral nucleus (CL), lateral posterior nucleus (LP), and VPs. Finally, thalamocortical connections of area 7b/AIP were from a range of nuclei including PA, PM, LP/LD, VL, CL, PL, and CM. The current data support two conclusions drawn from previous studies in titi monkeys and other primates. First, cortex caudal to area 1 in New World monkeys is more like area 5 than area 2. Second, the presence of thalamic input to area 5 from both motor nuclei and somatosensory nuclei of the thalamus, suggests that area 5 could be considered a highly specialized sensorimotor area. J. Comp. Neurol. 497:416–435, 2006.

Hand use and the evolution of posterior parietal cortex in primates

Primates have an expanded posterior parietal cortex compared to other mammals. However, this expansion varies across primate taxa so that the size complexity of posterior parietal cortex increases in proportion to overall brain and body size. while portions of posterior parietal cortex might be unique to primates, a region resembling area 5 has been identified in a variety of mammals. However, the connections and function of this area vary across mammals so that area 5 in rodents and primates may be homologous but not completely analogous. Most clearly, area 5 is much more specialized for hand use in primates.

Orientation selectivity in the visual cortex of the nine-banded armadillo

Orientation selectivity in primary visual cortex (V1) has been proposed to reflect a canonical computation performed by the neocortical circuitry. Although orientation selectivity has been reported in all mammals examined to date, the degree of selectivity and the functional organization of selectivity vary across mammalian clades. The differences in degree of orientation selectivity are large, from reports in marsupials that only a small subset of neurons are selective to studies in carnivores, in which it is rare to find a neuron lacking selectivity. Furthermore, the functional organization in cortex varies in that the primate and carnivore V1 is characterized by an organization in which nearby neurons share orientation preference while other mammals such as rodents and lagomorphs either lack or have only extremely weak clustering. To gain insight into the evolutionary emergence of orientation selectivity, we examined the nine-banded armadillo, a species within the early placental clade Xenarthra. Here we use a combination of neuroimaging, histological, and electrophysiological methods to identify the retinofugal pathways, locate V1, and for the first time examine the functional properties of V1 neurons in the armadillo (Dasypus novemcinctus) V1. Individual neurons were strongly sensitive to the orientation and often the direction of drifting gratings. We uncovered a wide range of orientation preferences but found a bias for horizontal gratings. The presence of strong orientation selectivity in armadillos suggests that the circuitry responsible for this computation is common to all placental mammals.NEW & NOTEWORTHY The current study shows that armadillo primary visual cortex (V1) neurons share the signature properties of V1 neurons of primates, carnivorans, and rodents. Furthermore, these neurons exhibit a degree of selectivity for stimulus orientation and motion direction similar to that found in primate V1. Our findings in armadillo visual cortex suggest that the functional properties of V1 neurons emerged early in the mammalian lineage, near the time of the divergence of marsupials.

Cortical connections of area 2 and posterior parietal area 5 in macaque monkeys

The overarching goal of the current investigation was to examine the connections of anterior parietal area 2 and the medial portion of posterior parietal area 5 in macaque monkeys; two areas that are part of a network involved reaching and grasping in primates. We injected neuroanatomical tracers into specified locations in each field and directly related labeled cells to histologically identified cortical field boundaries. Labeled cells were counted so that the relative density of projections to areas 2 and 5 from other cortical fields could be determined. Projections to area 2 were restricted and were predominantly from other somatosensory areas of the anterior parietal cortex (areas 1, 3b, and 3a), the second somatosensory area (S2), and from medial and lateral portions of area 5 (5M and 5L respectively). On the other hand, area 5M had very broadly distributed projections from a number of cortical areas including anterior parietal areas, from primary motor cortex (M1), premotor cortex (PM), the supplementary motor area (SMA), cortex on the medial wall, and from posterior parietal areas 5L and 7b. The more restricted pattern of connections of area 2 indicates that it processes somatic inputs locally and provides proprioceptive information to area 5M. 5M, which at least partially overlaps with functionally defined area MIP, receives inputs from somatosensory (predominantly from area 2), posterior parietal and motor cortex, which could provide the substrate for representing multiple coordinate systems necessary for planning ethologically relevant movements, particularly those involving the hand.