Cortical maps as a fundamental neural substrate for visual representation.

Visual perception is the product of serial hierarchical processing, parallel processing, and remapping on a dynamic network involving several topographically organized cortical visual areas. Here, we will focus on the topographical organization of cortical areas and the different kinds of visual maps found in the primate brain. We will interpret our findings in light of a broader representational framework for perception. Based on neurophysiological data, our results do not support the notion that vision can be explained by a strict representational model, where the objective visual world is faithfully represented in our brain. On the contrary, we find strong evidence that vision is an active and constructive process from the very initial stages taking place in the eye and from the very initial stages of our development. A constructive interplay between perceptual and motor systems (e.g., during saccadic eye movements) is actively learnt from early infancy and ultimately provides our fluid stable visual perception of the world.

Architecture of the inferior parietal cortex in capuchin monkey.

We studied the organization of the inferior parietal cortex (IPC) in five capuchin monkey (6 hemispheres) using cytoarchitectonic (Nissl), myeloarchitectonic (Gallyas), and immune-architectonic (SMI-32 monoclonal antibody) techniques. We partitioned the IPC into five distinct areas: PFG, PG, Opt, PFop, and PGop. Since we used parasagittal sections, we were not able to study area PF due to its far lateral position, which yielded slices that were tangential to the pial surface. Areas PFG, PG, and Opt were in the convexity close to the lateral sulcus, while PFop and PGop were positioned more posteriorly, in the opercular region of IPC. Of all the five regions, area Opt was the one most similar to its analogue in the macaque, especially as revealed with SMI-32 staining. Namely, in both primate species area Opt showed a low density of large pyramidal neurons. Additionally, the apical dendrites of these neurons were sparse and vertically orientated, resembling columns. We also found area PG to be similar: both species exhibited cell body layers with a radial arrangement. On the other hand, Nissl staining revealed area PFG to be architectonically different between New and Old-World monkeys: PFG in the capuchin showed a comparatively higher cell density than in macaques, especially in layers II and IV. These results suggest that evolution may have enabled the functional specialization of these brain regions based on behavioral demands of upper limb use. The small differences in the IPC of the two primates may be linked to interspecies variability.

Time course of dorsolateral geniculate nucleus plasticity in adult monkeys with laser-induced retinal lesions.

We studied changes in the expression of growth-associated protein 43 (GAP43), glial fibrillary acidic protein (GFAP), and calcium-binding proteins (calbindin [Cb] and parvalbumin [Pv]) in the dorsal lateral geniculate nucleus (dLGN) of four capuchin monkeys with laser-induced retinal lesions. The lesions were generated with the aid of a neodymium-YAG dual-frequency laser with shots of different intensity and at different survival time in each animal. The expression of these proteins in the layers of the dLGN was evaluated by performing histodensitometry of coronal sections throughout the nucleus. High-power laser shots administered at the border of the optic disc (OD)-injured fibers resulted in large scotomas. These lesions produced a devastating effect on fibers in this passage, resulting in large deafferentation of the dLGN. The time course of plasticity expressed in this nucleus varied with the degree of the retinal lesion. Topographically, corresponding portions of the dLGN were inferred by the extent of the ocular dominance column revealed by cytochrome oxidase histochemistry in flattened preparations of V1. In the region representing the retinal lesion, the expression of GFAP, GAP43, Pv, and Cb increased and decreased in the corresponding dLGN layers shortly after lesion induction and returned to their original values with different time courses. Synaptogenesis (indicated by GAP43 expression) appeared to be increased in all layers, while "cleansing" of the glial-damaged region (indicated by GFAP expression) was markedly greater in the parvocellular layers, followed by the magnocellular layers. Schematic drawings of optic discs laser lesions and of series of coronal sections of the dLGN, in three monkeys, depicting the areas of the nucleus deafferented by the lesions.

Effects of MT lesions on visuomotor performance in macaques.

Monkeys with selective bilateral lesions of area MT were trained on tasks designed to examine visuomotor function. They were required to: 1- retrieve a small food pellet from a narrow slot; 2- locate and retrieve a loose peanut mounted on a background of fixed peanuts; and 3- retrieve an erratically moving food pellet from a spinning bowl. After the lesions, these monkeys were behaviorally impaired relative to their own preoperative performances and also relative to the postoperative performances of the control monkeys with lesions in optic radiation fibers (OR) under MT or lesions in the posterior parietal cortex (PP). Although their performance improved with practice and time, the MT-lesioned monkeys showed long-term impairments twenty weeks after surgery. Control monkeys performed no worse on the tasks after their lesions. Another task which required the monkeys to retrieve a food pellet without visual guidance revealed that all the animals performed equally poorly when visual cues were unavailable, but that only the control monkeys benefited when visual cues were available. None of the monkeys were impaired on a pattern discrimination learning task. Besides that, direct observations revealed that the MT-lesioned animals grasped peanuts in a manner different from the control animals.

Genetic variability of the sws1 cone opsin gene among New World monkeys.

Vision is a major sense for Primates and the ability to perceive colors has great importance for the species ecology and behavior. Visual processing begins with the activation of the visual opsins in the retina, and the spectral absorption peaks are highly variable among species. In most Primates, LWS/MWS opsins are responsible for sensitivity to long/middle wavelengths within the visible light spectrum, and SWS1 opsins provide sensitivity to short wavelengths, in the violet region of the spectrum. In this study, we aimed to investigate the genetic variation on the sws1 opsin gene of New World monkeys (NWM) and search for amino acid substitutions that might be associated with the different color vision phenotypes described for a few species. We sequenced the exon 1 of the sws1 opsin gene of seven species from the families Callitrichidae, Cebidae, and Atelidae, and searched for variation at the spectral tuning sites 46, 49, 52, 86, 90, 93, 114, 116, and 118. Among the known spectral tuning sites, only residue 114 was variable. To investigate whether other residues have a functional role in the SWS1 absorption peak, we performed computational modeling of wild-type SWS1 and mutants A50I and A50V, found naturally among the species investigated. Although in silico analysis did not show any visible effect caused by these substitutions, it is possible that interactions of residue 50 with other sites might have some effect in the spectral shifts in the order of ~14 nm, found among the NWM. We also performed phylogenetic reconstruction of the sws1 gene, which partially recovered the species phylogeny. Further studies will be important to uncover the mutations responsible for the phenotypic variability of the SWS1 of NWM, and how spectral tuning may be associated with specific ecological features such as preferred food items and habitat use.

Tangential distribution of cell type and direction selectivity in monkey area MT.

We studied the multiunit responses to moving and static stimuli from 585 cell clusters in area MT using multi-electrode arrays. Our aim was to explore if MT columns exhibit any larger-scale tangential organization or clustering based on their response properties. Neurons showing both motion and orientation selectivity were classified into four categories: 1- Type I (orientation selectivity orthogonal to the axis of motion); 2- Type II (orientation selectivity coaxial to the axis of motion); 3- Type DS (significant response to moving stimuli, but non-significant response to static stimuli); and 4- Type OS (significant orientation selectivity, but non-significant direction selectivity). Type I (34%), Type II (24%) and Type DS (32%) clusters were the most predominant and may be associated with different stages of motion processing in MT. On the other hand, the rarer Type OS (9%) may be integrating motion and form processing. Type I and unidirectional sites were the only classes to exhibit significant clustering. Type OS sites showed a trend for clustering, which did not reach statistical significance. We also found a trend for unidirectional sites to have bidirectional sites as neighbors. In conclusion, neuronal clustering associated with these four categories may be related to distinct MT functional circuits.

Time course of cytochrome oxidase blob plasticity in the primary visual cortex of adult monkeys after retinal laser lesions.

We studied the time course of changes of cytochrome oxidase (CytOx) blob spatial density and blob cross-sectional area of deprived (D) and nondeprived (ND) portions of V1 in four capuchin monkeys after massive and restricted retinal laser lesions. Laser shots at the border of the optic disc produced massive retinal lesions, while low power laser shots in the retina produced restricted retinal lesions. These massive and restricted retinal lesions were intended to simulate glaucoma and diabetic retinopathy, respectively. We used a Neodymium-YAG dual frequency laser to make the lesions. We measured Layer III blobs in CytOx-reacted tangential sections of flat-mounted preparations of V1. The plasticity of the blob system and that of the ocular dominance columns (ODC) varied with the degree of retinal lesions. We found that changes in the blob system were different from that of the ODC. Blob sizes changed drastically in the region corresponding to the retinal lesion. Blobs were larger and subjectively darker above and below the non deprived ODC than in the deprived columns. With restricted lesions, blobs corresponding to the ND columns had sizes similar to those from non-lesioned areas. In contrast, blobs corresponding to the deprived columns were smaller than those from nonlesioned areas. With massive lesions, ND blobs were larger than the deprived blobs. Plastic changes in blobs described here occur much earlier than previously described.

Partitioning of the primate intraparietal cortex based on connectivity pattern and immunohistochemistry for Cat-301 and SMI-32.

We propose a partitioning of the primate intraparietal sulcus (IPS) using immunoarchitectural and connectivity criteria. We studied the immunoarchitecture of the IPS areas in the capuchin monkey using Cat-301 and SMI-32 immunohistochemistry. In addition, we investigated the IPS projections to areas V4, TEO, PO, and MT using retrograde tracer injections in nine hemispheres of seven animals. The pattern and distribution of Cat-301 and SMI-32 immunostaining revealed multiple areas in the IPS, in the adjoining PO cleft and in the annectant gyrus, with differential staining patterns found for areas V3d, DM, V3A, DI, PO, POd, CIP-1, CIP-2, VIPa, VIPp, LIPva, LIPvp, LIPda, LIPdp, PIPv, PIPd, MIPv, MIPd, AIPda, AIPdp, and AIPv. Areas V4, TEO, PO, MT, which belong to different cortical streams of visual information processing, receive projections from at least twenty different areas within the IPS and adjoining regions. In six animals, we analyzed the distribution of retrogradely labeled cells in tangential sections of flat-mount IPS preparations. The lateral bank of the IPS projects to regions belonging both to the ventral (V4 and TEO) and dorsal (PO and MT) streams. The region on the floor of the IPS (i.e., VIP) projects predominantly to dorsal stream areas. Finally, the medial bank of the IPS (i.e., MIP) projects solely to the dorsalmedial stream (PO). Therefore, our data suggest that ventral and dorsal streams remain segregated within the IPS, and that its projections to the dorsal stream can be further segregated based on those targeting the dorsolateral versus the dorsomedial subdivisions.

Cortical Afferents of Area 10 in Cebus Monkeys: Implications for the Evolution of the Frontal Pole.

Area 10, located in the frontal pole, is a unique specialization of the primate cortex. We studied the cortical connections of area 10 in the New World Cebus monkey, using injections of retrograde tracers in different parts of this area. We found that injections throughout area 10 labeled neurons in a consistent set of areas in the dorsolateral, ventrolateral, orbital, and medial parts of the frontal cortex, superior temporal association cortex, and posterior cingulate/retrosplenial region. However, sites on the midline surface of area 10 received more substantial projections from the temporal lobe, including clear auditory connections, whereas those in more lateral parts received >90% of their afferents from other frontal areas. This difference in anatomical connectivity reflects functional connectivity findings in the human brain. The pattern of connections in Cebus is very similar to that observed in the Old World macaque monkey, despite >40 million years of evolutionary separation, but lacks some of the connections reported in the more closely related but smaller marmoset monkey. These findings suggest that the clearer segregation observed in the human frontal pole reflects regional differences already present in early simian primates, and that overall brain mass influences the pattern of cortico-cortical connectivity.

Neuronal response properties across cytochrome oxidase stripes in primate V2.

Cytochrome oxidase histochemistry reveals large-scale cortical modules in area V2 of primates known as thick, thin, and interstripes. Anatomical, electrophysiological, and tracing studies suggest that V2 cytochrome oxidase stripes participate in functionally distinct streams of visual information processing. However, there is controversy whether the different V2 compartments indeed correlate with specialized neuronal response properties. We used multiple-electrode arrays (16 × 2, 8 × 4 and 4 × 4 matrices) to simultaneously record the spiking activity (N = 190 single units) across distinct V2 stripes in anesthetized and paralyzed capuchin monkeys (N = 3 animals, 6 hemispheres). Visual stimulation consisted of moving bars and full-field gratings with different contrasts, orientations, directions of motion, spatial frequencies, velocities, and color contrasts. Interstripe neurons exhibited the strongest orientation and direction selectivities compared to the thick and thin stripes, with relatively stronger coding for orientation. Additionally, they responded best to higher spatial frequencies and to lower stimulus velocities. Thin stripes showed the highest proportion (80%) of neurons selective to color contrast (compared to 47% and 21% for thick and interstripes, respectively). The great majority of the color selective cells (86%) were also orientation selective. Additionally, thin stripe neurons continued to increase their firing rate for stimulus contrasts above 50%, while thick and interstripe neurons already exhibited some degree of response saturation at this point. Thick stripes best coded for lower spatial frequencies and higher stimulus velocities. In conclusion, V2 CytOx stripes exhibit a mixed degree of segregation and integration of information processing, shedding light into the early mechanisms of vision.

Introduction.

The pulvinar can be subdivided into well-delimitated regions based on chemoarchitectural, cytoarchitectural, myeloarchitectural, connectivity, and electrophysiological criteria. Subdivisions of the pulvinar based on its chemoarchitectural features are the most consistently preserved across species of New and Old World monkeys. It is reasonable to speculate that the occurrence and distribution of calcium-binding proteins in the pulvinar, such as calbindin and parvalbumin, have been preserved along evolution. Therefore, they have proven to be valuable tools capable of probing the basic pulvinar scaffold across primate species. Along this review, we will provide an overview of the available data regarding the various subdivisions of the pulvinar that have been proposed based on architectural criteria such as the distribution of molecular markers, neuronal morphology, and fiber layout.

Cytoarchitecture and Myeloarchitecture of the Pulvinar.

In this chapter, we discuss the different ways in which the primate pulvinar has been subdivided, based on cytoarchitectural and myeloarchitectural criteria. One original criterion, based on cytoarchitecture, subdivided the pulvinar into nucleus pulvinaris medialis (PM), nucleus pulvinaris lateralis (PL), and nucleus pulvinaris inferior (PI). Later, the anterior limits of the pulvinar were extended and a subdivision was added to this nucleus, named pulvinar oralis (PO). PO occupies the anterior portion of the pulvinar and appears between the nucleus centrum medianum (CM) and the nucleus ventralis posterior lateralis (VPL).

Chemoarchitecture of the Pulvinar.

Cytochemical and immunocytochemical methods reveal details of the pulvinar architecture that are not apparent from Nissl and myelin staining. The results of these techniques have been interpreted in different ways by different investigators, each adopting different sets of nomenclature for the various pulvinar subdivisions. In this chapter, we discuss the notion that the differentiation of the pulvinar along primate evolution took place upon a relatively rigid chemoarchitectonic scaffold.

Visual Map Representations in the Primate Pulvinar.

The pulvinar receives direct visual information from the retina and indirect visual information from several cortical and subcortical areas. In this chapter, we discuss the visuotopic organization of the primate pulvinar. Electrophysiological techniques have been systematically employed to study pulvinar visuotopy in the owl, capuchin, and macaque monkeys. A single map of the visual field has been described in the pulvinar of the owl monkey, while two independent maps have been described in the capuchin and macaque pulvinar.

Connectivity of the Pulvinar.

Pulvinar connectivity has been studied using a variety of neuroanatomical tracing techniques in both New and Old World monkeys. Connectivity studies have revealed additional maps of the visual field other than those described using electrophysiological techniques, such as P3 in the capuchin monkey and P3/P4 in the macaque monkey. In this chapter, we argue that with increasing cortical size, the pulvinar developed new functional subdivisions in order to effectively interconnect and interact with the cortex.

Reestablishing the Chemoarchitectural Borders Based on Electrophysiological and Connectivity Data.

In this chapter, we discuss the poor agreement between visuotopic maps described using electrophysiological and connectivity data and the subdivisions of the pulvinar based on chemoarchitecture. We focus on the differences and similarities between New and Old World monkeys to evaluate how this agreement evolved during evolution. There is some agreement in the localization of P1, described using electrophysiological and connectivity data, and the lateral and central portions of the nucleus pulvinaris inferior (PI), defined based on chemoarchitectural criteria. Similarly, there is some colocalization between P3 and the medial portion of PI in both New and Old World monkeys. One difference between primates refers to P2, which is present in the Old World macaque monkey but absent in the New World monkeys. P4, which has not been studied in all primates, shows a partial spatial agreement with the dorsal portion of the chemoarchitecturally defined PL.

Visual Topography of the Pulvinar Projection Zones.

In this chapter, we describe the visuotopy of the pulvinar subdivisions P1, P2, and P4. In all primates, P1 colocalizes with the chemoarchitecturally defined PI and a small portion of PL. The peripheral visual field is represented anteriorly in the medial portion of PI, while central vision is represented more posteriorly in the medial portion of PL. The vertical meridian representation is located on the lateral edge of P1, while the horizontal meridian is represented obliquely from the lateral to the medial extent of P1. The upper visual field is represented ventrally, while the lower field is located dorsally. P2 has only been described in the macaque monkey. It contains a representation of the peripheral visual field, located in its anterior portion, and of the central field, which is located in posterior PL. P4 has a complex topographic arrangement. The representation of the vertical meridian is located on the dorsal edge of P4, while the representation of the horizontal meridian divides P4 into dorsal and ventral portions.

Comparative Pulvinar Organization Across Different Primate Species.

In this chapter, we compare the pattern of pulvinar immunohistochemical staining for the calcium-binding proteins calbindin and parvalbumin and for the neurofilament protein SMI-32 in macaque, capuchin, and squirrel monkeys. This group of New and Old World primates shares five similar pulvinar subdivisions: PIP, PIM, PIC, PIL, and PILS. In the Old World macaque monkey, the inferior-lateral pulvinar can be subdivided into the P1 and P2 fields based on its connectivity with visual area V1. On the other hand, only the P1 field and no P2 was found in the New World capuchin monkey. Notably, the similarities in chemoarchitecture contrast with the distinct connectivity patterns and the different visuotopic organizations found across the species.

Response Properties of Pulvinar Neurons Studied with Single-Unit Electrophysiological Recordings.

In this chapter, we discuss the types of visual receptive fields revealed by single-unit electrophysiological recordings in the pulvinar. Nearly all neurons with identifiable receptive fields responded to visual stimulation presented on the contralateral hemifield, within 25° of the fovea. The majority of the visual neurons responded to some form of moving stimulus, and some additionally exhibited direction or orientation selectivity. Most units could be driven by monocular stimulation and showed receptive fields of at least 100 square degrees in area. Finally, most of the units recorded exhibited continuous peripheral receptive fields, even though a few of them could be bilaterally activated.

Modulation of Pulvinar Neuronal Activity by Arousal.

In this chapter, we discuss the modulation of pulvinar neuronal activity by arousal. In contrast to electrophysiological recordings in the early visual cortex, neuronal activity in the pulvinar is particularly sensitive to anesthesia. In the absence of sensory stimulation, pulvinar neurons can be characterized by spontaneous low-frequency rhythmic bursts of spiking activity. However, multisensory stimulation capable of arousing the animal from deeper anesthesia levels is able to reestablish the necessary neuronal dynamics and switch the pulvinar into an active state. Under these conditions, cortical slow-wave activity is substituted by a higher-frequency oscillatory pattern associated with arousal. Here, we describe two types of transitions in pulvinar activity pattern that can be observed when arousing the animal with multisensory stimulation.