Mario Fiorani

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.

Cortical afferents of visual area MT in the Cebus monkey: possible homologies between new and old world monkeys

Cortical projections to the middle temporal (MT) visual area were studied by injecting the retrogradely transported fluorescent tracer Fast Blue into MT in adult New World monkeys (Cebus apella). Injection sites were selected based on electrophysiological recordings, and covered eccentricities from 2-70 deg, in both the upper and lower visual fields. The position and laminar distribution of labeled cell bodies were correlated with myeloarchitectonic boundaries and displayed in flat reconstructions of the neocortex. Topographically organized projections were found to arise mainly from the primary, second, third, and fourth visual areas (V1, V2, V3, and V4). Coarsely topographic patterns were observed in transitional V4 (V4t), in the parieto-occipital and parieto-occipital medial areas (PO and POm), and in the temporal ventral posterior area (TVP). In addition, widespread or nontopographic label was found in visual areas of the superior temporal sulcus (medial superior temporal, MST, and fundus of superior temporal, FST), annectent gyrus (dorsointermediate area, DI; and dorsomedial area, DM), intraparietal sulcus (lateral intraparietal, LIP; posterior intraparietal, PIP; and ventral intraparietal, VIP), and in the frontal eye field (FEF). Label in PO, POm, and PIP was found only after injections in the representation of the peripheral visual field (> 10 deg), and label in V4 and FST was more extensive after injections in the central representation. The projections from V1 and V2 originated predominantly from neurons in supragranular layers, whereas those from V3, V4t, DM, DI, POm, and FEF consisted of intermixed patches with either supragranular or infragranular predominance. All of the other projections were predominantly infragranular. Invasion of area MST by the injection site led to the labeling of further pathways, including substantial projections from the dorsal prelunate area (DP) and from an ensemble of areas located along the medial wall of the hemisphere. In addition, weaker projections were observed from the parieto-occipital dorsal area (POd), area 7a, area prostriata, the posterior bank of the arcuate sulcus, and areas in the anterior part of the lateral sulcus. Despite the different nomenclatures and areal boundaries recognized by different models of simian cortical organization, the pattern of projections to area MT is remarkably similar among primates. Our results provide evidence for the existence of many homologous areas in the extrastriate visual cortex of New and Old World monkeys.

Complete pattern of ocular dominance stripes in V1 of a New World monkey, Cebus apella

SummaryThe presence of ocular dominance (OD) stripes in layer IVc of striate cortex (V1) is characteristic of all Old World simians so far studied. In contrast, some species of New World monkeys do not have ocular dominance stripes, and in those that do, the pattern of stripes may be different from that shown in Old World monkeys. This difference has led to the suggestion that OD stripes evolved independently in both groups. We have mapped the entire system of OD stripes in the New World monkey Cebus, by means of cytochrome oxidase histochemistry after monocular enucleation. A striking similarity was found between the patterns in Cebus and Macaca, which is suggestive of common ancestry, rather than parallel evolution.

Connectional and neurochemical subdivisions of the pulvinar in Cebus monkeys

Based on cytoarchitectonic criteria, the primate pulvinar nucleus has been subdivided into medial (PM), lateral (PL), and inferior (PI) regions. However, these subdivisions show no correlation with those established by electrophysiological, immunocytochemical, or neuroanatomical tracer studies. In this work, we studied the connections of the pulvinar nucleus of Cebus monkey with visual areas V1, V2, V4, MT, and PO by means of retrograde fluorescent tracers injected into these areas. Based on the projection zones to cortical visual areas, the visual portion of the pulvinar of Cebus monkey was subdivided into three subregions: P1, P2, and P3, similar to those described in the macaque (Ungerleider et al., 1984). In Cebus, P1 includes the centrolateral portion of traditionally defined PI and adjacent portion of PL. P2 is located in the dorsal portion of PL and P3 includes the medial portion of PI and extends dorsally into adjacent PL and PM. In addition, we studied the histology of the pulvinar using multiple criteria, such as cytoarchitecture and myeloarchitecture; histochemistry for cytochrome oxidase, NADPH-diaphorase, and acetylcholinesterase; and immunocytochemistry for two calcium-binding proteins, calbindin and parvalbumin, and for a neurofilament recognized by the SMI-32 antibody. Some of these stains, mainly calbindin, showed additional subdivisions of the Cebus pulvinar, beyond the traditional PI, PL, and PM. Based on this immunohistochemical staining, the border of PI is moved dorsally above the brachium of the superior colliculus and PI can be subdivided in five regions (PI(P), PI(M), PI(C), PI(L), and PI(LS)). Regions P1, P2, and P3 defined based on efferent connections with cortical visual areas are not architectonically/neurochemically homogeneous. Rather they appear to consist of further chemoarchitectonic subdivisions. These distinct histochemical regions might be related to different functional modules of visual processing within one connectional area.

Quantification of Early Stages of Cortical Reorganization of the Topographic Map of V1 Following Retinal Lesions in Monkeys

We quantified the capacity for reorganization of the topographic representation of area V1 in adult monkeys. Bias-free automated mapping methods were used to delineate receptive fields (RFs) of an array of neuronal clusters prior to, and up to 6 h following retinal lesions. Monocular lesions caused a significant reorganization of the topographic map in this area, both inside and outside the cortical lesion projection zone (LPZ). Small flashed stimuli revealed responses up to 0.85 mm inside the boundaries of the LPZ, with RFs representing regions of undamaged retina immediately surrounding the lesion. In contrast, long moving bars that spanned the scotoma resulting from the lesion revealed responsive units up to 1.87 mm inside the LPZ, with RFs representing interpolated responses in this region. This reorganization is present immediately after monocular retinal lesioning. Both stimuli showed a similar and significant (5-fold) increase of the RF scatter in the LPZ, 0.56 mm (median), compared with the undamaged retina, 0.12 mm. Our results reveal an array of preexisting subthreshold functional connections of up to 2 mm in V1, which can be rapidly mobilized independently from the differential qualitative reorganization elicited by each stimulus.

Effects of inactivation of the lateral pulvinar on response properties of second visual area cells in Cebus monkeys.

1. In the present study, we investigated the influence of the pulvinar nucleus upon response properties of single cells in the second visual area (V2) of Cebus monkeys. The method used consisted of the inactivation of a portion of the lateral pulvinar by GABA injections while studying the response properties of cells in V2 at the same visuotopic location as that of the inactivation.

Cone photopigment variations in Cebus apella monkeys evidenced by electroretinogram measurements and genetic analysis.

We investigated the color vision pattern in Cebus apella monkeys by means of electroretinogram measurements (ERG) and genetic analysis. Based on ERG we could discriminate among three types of dichromatic males. Among females, this classification is more complex and requires additional genetic analysis. We found five among 10 possible different phenotypes, two trichromats and three dichromats. We also found that Cebus present a new allele with spectral peak near 552nm, with the amino acid combination SFT at positions 180, 277 and 285 of the opsin gene, in addition to the previously described SYT, AFT and AFA alleles.

Differential expression of Zif268 and c-Fos in the primary visual cortex and lateral geniculate nucleus of normal Cebus monkeys and after monocular lesions.

The transcription factors c‐Fos and Zif268 have been used as markers of neuronal activity, and they also have been implicated in neuronal plasticity. In this study, we investigated the expression of c‐Fos and Zif268 proteins in the lateral geniculate nucleus (LGN) and in the cortical primary visual area (V1) of normal adult Cebus apella monkeys and in animals with monocular lesions. In the LGN, the reaction for c‐Fos showed immunopositive cells in both magnocellular (M) and parvocellular (P) layers; however, the label was heavier in P layers. In animals that suffered monocular lesions, the immunocytochemistry for c‐Fos showed more labeling in layers related to the normal eye compared with those of the lesioned eye. No specific label was observed after the reaction for Zif268 in the LGN. In V1, the reaction for both Zif268 and c‐Fos showed a pattern of lamination in which heavier labeling was found in layers 2/3, 4A, 4C, and 6. After monocular lesions, we observed a clear pattern of ocular dominance columns in V1 for both c‐Fos and Zif268, in which the columns related to the normal eye are more heavily labeled than those related to the lesioned eye. This pattern is more evident in layer 4C after c‐Fos reaction, whereas, after Zif268, it is more clearly observed in layers 2/3. These results suggest that, in addition to be regulated by functional activity, these transcription factors are involved in different processes during cortical reorganization. J. Comp. Neurol. 482:166–175, 2005.

Distribution of neurofilament proteins in the lateral geniculate nucleus, primary visual cortex, and area MT of adult Cebus monkeys

We investigated the distribution pattern of SMI‐32‐immunopositive cells in the lateral geniculate nucleus (LGN) and in the primary (V1) and middle temporal (MT) cortical visual areas of the adult New World monkey Cebus apella. In the LGN, the reaction for SMI‐32 labeled cells in both the magnocellular (M) and parvocellular (P) layers. However, the cellular label was heavier in M layers, which also showed a more intense labeling in the neuropil. In V1, the reaction showed a lamination pattern, with the heaviest labeling occurring in layer 4B and upper layer 6 (layers that project to area MT). Area MT shows a dense band of labeled neuropil and large pyramidal neurons in layer 3, large darkly labeled but less densely packed neurons in layer 5, and a population of small, lightly labeled cells in layer 6. These results resemble those found in other New and Old World monkeys, which suggest that the preferential labeling of projection neurons associated with fast‐conducting pathways to the extrastriate dorsal stream is a common characteristic of simian primates. In the superficial layers of V1 in Cebus monkeys, however, SMI‐32‐labeled neurons are found in both cytochrome oxidase blobs and interblob regions. In this aspect, our results in Cebus are similar to those found in the Old World monkey Macaca and different from those described for squirrel monkey, a smaller New World Monkey. In Cebus, as well as in Macaca, there is no correlation between SMI‐32 distribution and the blob pattern. J. Comp. Neurol. 508:605–614, 2008.

Visual Responses Outside the Classical Receptive Field in Primate Striate Cortex: A Possible Correlate of Perceptual Completion

In this chapter we address the dynamic properties of single neurons in primary visual cortex (V1) that can be related to the completion phenomenon. This phenomenon accounts for the perceptual filling in of blind regions in the visual field, such as the optic disk, small retinal lesions (Bender and Teuber, 1946; Sergent, 1988), or lesions in the geniculo-striatal projection system (Poppel, 1985, 1986). We propose that completion is achieved by dynamic changes in receptive field size of cells in V1.