Visual thalamocortical projections in the flying fox: Parallel pathways to striate and extrastriate areas

We studied thalamic projections to the visual cortex in flying foxes, animals that share neural features believed to resemble those present in the brains of early primates. Neurones labeled by injections of fluorescent tracers in striate and extrastriate cortices were charted relative to the architectural boundaries of thalamic nuclei. Three main findings are reported: First, there are parallel lateral geniculate nucleus (LGN) projections to striate and extrastriate cortices. Second, the pulvinar complex is expansive, and contains multiple subdivisions. Third, across the visual thalamus, the location of cells labeled after visual cortex injections changes systematically, with caudal visual areas receiving their strongest projections from the most lateral thalamic nuclei, and rostral areas receiving strong projections from medial nuclei. We identified three architectural layers in the LGN, and three subdivisions of the pulvinar complex. The outer LGN layer contained the largest cells, and had strong projections to the areas V1, V2 and V3. Neurones in the intermediate LGN layer were intermediate in size, and projected to V1 and, less densely, to V2. The layer nearest to the origin of the optic radiation contained the smallest cells, and projected not only to V1, V2 and V3, but also, weakly, to the occipitotemporal area (OT, which is similar to primate middle temporal area) and the occipitoparietal area (OP, a third tier area located near the dorsal midline). V1, V2 and V3 received strong projections from the lateral and intermediate subdivisions of the pulvinar complex, while OP and OT received their main thalamic input from the intermediate and medial subdivisions of the pulvinar complex. These results suggest parallels with the carnivore visual system, and indicate that the restriction of the projections of the large- and intermediatesized LGN layers to V1, observed in present-day primates, evolved from a more generalized mammalian condition. (C) 2004 IBRO. Published by Elsevier Ltd. All rights reserved.

First- and second-order stimulus length selectivity in New World monkey striate cortex

Motion is a powerful cue for figure-ground segregation, allowing the recognition of shapes even if the luminance and texture characteristics of the stimulus and background are matched. In order to investigate the neural processes underlying early stages of the cue-invariant processing of form, we compared the responses of neurons in the striate cortex (V1) of anaesthetized marmosets to two types of moving stimuli: bars defined by differences in luminance, and bars defined solely by the coherent motion of random patterns that matched the texture and temporal modulation of the background. A population of form-cue-invariant (FCI) neurons was identified, which demonstrated similar tuning to the length of contours defined by first- and second-order cues. FCI neurons were relatively common in the supragranular layers (where they corresponded to 28% of the recorded units), but were absent from layer 4. Most had complex receptive fields, which were significantly larger than those of other V1 neurons. The majority of FCI neurons demonstrated end-inhibition in response to long first- and second-order bars, and were strongly direction selective, Thus, even at the level of V1 there are cells whose variations in response level appear to be determined by the shape and motion of the entire second-order object, rather than by its parts (i.e. the individual textural components). These results are compatible with the existence of an output channel from V1 to the ventral stream of extrastriate areas, which already encodes the basic building blocks of the image in an invariant manner.

Regional specialization in pyramidal cell structure in the visual cortex of the galago: An intracellular injection study of striate and extrastriate areas with comparative notes on New World and Old World monkeys

Recent studies have revealed marked differences in the basal dendritic structure of layer III pyramidal cells in the cerebral cortex of adult simian primates. In particular, there is a consistent trend for pyramidal cells of increasing complexity with anterior progression through occipitotemporal cortical visual areas. These differences in pyramidal cell structure, and their systematic nature, are believed to be important for specialized aspects of visual processing within, and between, cortical areas. However, it remains unknown whether this regional specialization in the pyramidal cell phenotype is unique to simians, is unique to primates in general or is widespread amongst mammalian species. In the present study we investigated pyramidal cell structure in the prosimian galago (Otolemur garnetti). We found, as in simians, that the basal dendritic arbors of pyramidal cells differed between cortical areas. More specifically, pyramidal cells became progressively more spinous through the primary (V1), second (V2), dorsolateral (DL) and inferotemporal ( IT) visual areas. Moreover, pyramidal neurons in V1 of the galago are remarkably similar to those in other primate species, in spite of large differences in the sizes of this area. In contrast, pyramidal cells in inferotemporal cortex are quite variable among primate species. These data suggest that regional specialization in pyramidal cell phenotype was a likely feature of cortex in a common ancestor of simian and prosimian primates, but the degree of specialization varies between species. Copyright (C) 2005 S. Karger AG, Basel.

Spontaneous and stimulus-evoked intrinsic optical signals in primary auditory cortex of the cat

Spontaneous and tone-evoked changes in light reflectance were recorded from primary auditory cortex (A1) of anesthetized cats (barbiturate induction, ketamine maintenance). Spontaneous 0.1-Hz oscillations of reflectance of 540- and 690-nm light were recorded in quiet. Stimulation with tone pips evoked localized reflectance decreases at 540 nm in 3/10 cats. The distribution of patches activated by tones of different frequencies reflected the known tonotopic organization of auditory cortex. Stimulus-evoked reflectance changes at 690 nm were observed in 9/10 cats but lacked stimulus-dependent topography. In two experiments, stimulus-evoked optical signals at 540 nm were compared with multiunit responses to the same stimuli recorded at multiple sites. A significant correlation (P < 0.05) between magnitude of reflectance decrease and multiunit response strength was evident in only one of five stimulus conditions in each experiment. There was no significant correlation when data were pooled across all stimulus conditions in either experiment. In one experiment, the spatial distribution of activated patches, evident in records of spontaneous activity at 540 nm, was similar to that of patches activated by tonal stimuli. These results suggest that local cerebral blood volume changes reflect the gross tonotopic organization of A1 but are not restricted to the sites of spiking neurons.

Pyramidal neurones in macaque visual cortex: Interareal phenotypic variation of dendritic branching patterns

The basal dendritic arbors of over 500-layer III pyramidal neurones of the macaque cortex were compared by fractal analyses, which provides a measure of the space filling (or branching pattern) of dendritic arbors. Fractal values (D) of individual cells were compared between the cytochrome oxidase (CO)-rich blobs and CO-poor interblobs, of middle and upper layer III, and between sublaminae, in the primary visual area (Vi). These data were compared with those in the CO compartments in the second visual area (V2), and seven other extrastriate cortical areas. (V4, MT, LIP, 7a, TEO, TE and STP). There were significant differences in the fractal dimensions, and therefore the dendritic branching patterns, of cells in striate and extrastriate areas. Of the 55 possible pairwise comparisons of fractal dimension of neurones in different cortical areas (or CO compartments), 39 proved to be significantly different. The markedly different morphologies of pyramidal cells in the different cortical areas may be one of the features that determine the functional signatures of these cells by influencing the number of inputs received by, and propagation of potentials through, their dendritic arbors.

Interlaminar differences in the pyramidal cell phenotype in cortical areas 7m and STP (the superior temporal polysensory area) of the macaque monkey

Pyramidal neurones were injected with Lucifer Yellow in slices cut tangential to the surface of area 7m and the superior temporal polysensory area (STP) of the macaque monkey. Comparison of the basal dendritic arbors of supra- and infragranular pyramidal neurones (n=139) that were injected in the same putative modules in the different cortical areas revealed variation in their structure. Moreover, there were relative differences in dendritic morphology of supra- and infragranular pyramidal neurones in the two cortical areas. Shell analyses revealed that layer III pyramidal neurones in area STP had considerably higher peak complexity (maximum number of dendritic intersections per Shell circle) than those in layer V, whereas peak complexities were similar for supra- and infragranular pyramidal neurones in area 7m. In both cortical areas, the basal dendritic trees of layer m pyramidal neurones were characterized by a higher spine density than those in layer V. Calculations of the total number of dendritic spines in the average basal dendritic arbor revealed that layer V pyramidal neurones in area 7m had twice as many spines as cells in layer III. (4535 and 2294, respectively). A similar calculation for neurones in area STP revealed that layer III pyramidal neurones had approximately the same number of spines as cells in layer V (3585 and 3850 spines, respectively). Relative differences in the branching patterns of, and the number of spines in, the basal dendritic arbors of supra- and infragranular pyramidal neurones in the different cortical areas may allow for integration of different numbers of inputs, and different degrees of dendritic processing. These results support the thesis that intra-areal circuitry differs in different cortical areas.

Linear models of simple cells: Correspondence to real cell responses and space spanning properties

Despite their limitations, linear filter models continue to be used to simulate the receptive field properties of cortical simple cells. For theoreticians interested in large scale models of visual cortex, a family of self-similar filters represents a convenient way in which to characterise simple cells in one basic model. This paper reviews research on the suitability of such models, and goes on to advance biologically motivated reasons for adopting a particular group of models in preference to all others. In particular, the paper describes why the Gabor model, so often used in network simulations, should be dropped in favour of a Cauchy model, both on the grounds of frequency response and mutual filter orthogonality.

Dendritic branching of pyramidal cells in the visual cortex of the nocturnal owl monkey: A fractal analysis

The branching structure of neurones is thought to influence patterns of connectivity and how inputs are integrated within the arbor. Recent studies have revealed a remarkable degree of variation in the branching structure of pyramidal cells in the cerebral cortex of diurnal primates, suggesting regional specialization in neuronal function. Such specialization in pyramidal cell structure may be important for various aspects of visual function, such as object recognition and color processing. To better understand the functional role of regional variation in the pyramidal cell phenotype in visual processing, we determined the complexity of the dendritic branching pattern of pyramidal cells in visual cortex of the nocturnal New World owl monkey. We used the fractal dilation method to quantify the branching structure of pyramidal cells in the primary visual area (V1), the second visual area (V2) and the caudal and rostral subdivisions of inferotemporal cortex (ITc and ITr, respectively), which are often associated with color processing. We found that, as in diurnal monkeys, there was a trend for cells of increasing fractal dimension with progression through these cortical areas. The increasing complexity paralleled a trend for increasing symmetry. That we found a similar trend in both diurnal and nocturnal monkeys suggests that it was a feature of a common anthropoid ancestor.

Topographic plasticity in primary visual cortex is mediated by local corticocortical connections

The placement of monocular laser lesions in the adult cat retina produces a lesion projection zone (LPZ) in primary visual cortex (V1) in which the majority of neurons have a normally located receptive field (RF) for stimulation of the intact eye and an ectopically located RF ( displaced to intact retina at the edge of the lesion) for stimulation of the lesioned eye. Animals that had such lesions for 14 - 85 d were studied under halothane and nitrous oxide anesthesia with conventional neurophysiological recording techniques and stimulation of moving light bars. Previous work suggested that a candidate source of input, which could account for the development of the ectopic RFs, was long-range horizontal connections within V1. The critical contribution of such input was examined by placing a pipette containing the neurotoxin kainic acid at a site in the normal V1 visual representation that overlapped with the ectopic RF recorded at a site within the LPZ. Continuation of well defined responses to stimulation of the intact eye served as a control against direct effects of the kainic acid at the LPZ recording site. In six of seven cases examined, kainic acid deactivation of neurons at the injection site blocked responsiveness to lesioned-eye stimulation at the ectopic RF for the LPZ recording site. We therefore conclude that long-range horizontal projections contribute to the dominant input underlying the capacity for retinal lesion-induced plasticity in V1.

Bi-sensory, striped representations: comparative insights from owl and platypus

Bi-sensory striped arrays are described in owl and platypus that share some similarities with the other variant of bi-sensory striped array found in primate and carnivore striate cortex: ocular dominance columns. Like ocular dominance columns, the owl and platypus striped systems each involve two different topographic arrays that are cut into parallel stripes, and interdigitated, so that higher-order neurons can integrate across both arrays. Unlike ocular dominance stripes, which have a separate array for each eye, the striped array in the middle third of the owl tectum has a separate array for each cerebral hemisphere. Binocular neurons send outputs from both hemispheres to the striped array where they are segregated into parallel stripes according to hemisphere of origin. In platypus primary somatosensory cortex (SI), the two arrays of interdigitated stripes are derived from separate sensory systems in the bill, 40,000 electroreceptors and 60,000 mechanoreceptors. The stripes in platypus SI cortex produce bimodal electrosensory-mechanosensory neurons with specificity for the time-of-arrival difference between the two systems. This thunder-and-lightning system would allow the platypus to estimate the distance of the prey using time disparities generated at the bill between the earlier electrical wave and the later mechanical wave caused by the motion of benthic prey. The functional significance of parallel, striped arrays is not clear, even for the highly-studied ocular dominance system, but a general strategy is proposed here that is based on the detection of temporal disparities between the two arrays that can be used to estimate distance. (C) 2004 Elsevier Ltd. All rights reserved.

Fractal analysis of pyramidal cells in the visual cortex of the galago (Otolemur garnetti): Regional variation in dendritic branching patterns between visual areas

Previously it has been shown that the branching pattern of pyramidal cells varies markedly between different cortical areas in simian primates. These differences are thought to influence the functional complexity of the cells. In particular, there is a progressive increase in the fractal dimension of pyramidal cells with anterior progression through cortical areas in the occipitotemporal (OT) visual stream, including the primary visual area (V1), the second visual area (V2), the dorsolateral area (DL, corresponding to the fourth visual area) and inferotemporal cortex (IT). However, there are as yet no data on the fractal dimension of these neurons in prosimian primates. Here we focused on the nocturnal prosimian galago (Otolemur garnetti). The fractal dimension (D), and aspect ratio (a measure of branching symmetry), was determined for I I I layer III pyramidal cells in V1, V2, DL and IT. We found, as in simian primates, that the fractal dimension of neurons increased with anterior progression from V1 through V2, DL, and IT. Two important conclusions can be drawn from these results: (1) the trend for increasing branching complexity with anterior progression through OT areas was likely to be present in a common primate ancestor, and (2) specialization in neuron structure more likely facilitates object recognition than spectral processing.

Pyramidal neurons of granular prefrontal cortex of the galago: Complexity in evolution of the psychic cell in primates

Typically, cognitive abilities of humans have been attributed to their greatly expanded cortical mantle, granular prefrontal cortex (gPFC) in particular. Recently we have demonstrated systematic differences in microstructure of gPFC in different species. Specifically, pyramidal cells in adult human gPFC are considerably more spinous than those in the gPFC of the macaque monkey, which are more spinous than those in the gPFC of marmoset and owl monkeys. As most cortical dendritic spines receive at least one excitatory input, pyramidal cells in these different species putatively receive different numbers of inputs. These differences in the gPFC pyramidal cell phenotype may be of fundamental importance in determining the functional characteristics of prefrontal circuitry and hence the cognitive styles of the different species. However, it remains unknown as to why the gPFC pyramidal cell phenotype differs between species. Differences could be attributed to, among other things, brain size, relative size of gPFC, or the lineage to which the species belong. Here we investigated pyramidal cells in the dorsolateral gPFC of the prosimian galago to extend the basis for comparison. We found these cells to be less spinous than those in human, macaque, and marmoset. (c) 2005 Wiley-Liss, Inc.

Areal specialization of pyramidal cell structure in the visual cortex of the tree shrew: a new twist revealed in the evolution of cortical circuitry

Cortical pyramidal cells, while having a characteristic morphology, show marked phenotypic variation in primates. Differences have been reported in their size, branching structure and spine density between cortical areas. In particular, there is a systematic increase in the complexity of the structure of pyramidal cells with anterior progression through occipito-temporal cortical visual areas. These differences reflect area-specific specializations in cortical circuitry, which are believed to be important for visual processing. However, it remains unknown as to whether these regional specializations in pyramidal cell structure are restricted to primates. Here we investigated pyramidal cell structure in the visual cortex of the tree shrew, including the primary (V1), second (V2) and temporal dorsal (TD) areas. As in primates, there was a trend for more complex branching structure with anterior progression through visual areas in the tree shrew. However, contrary to the trend reported in primates, cells in the tree shrew tended to become smaller with anterior progression through V1, V2 and TD. In addition, pyramidal cells in V1 of the tree shrew are more than twice as spinous as those in primates. These data suggest that variables that shape the structure of adult cortical pyramidal cells differ among species.

Resolving the organization of the New World monkey third visual complex: The dorsal extrastriate cortex of the marmoset (Callithrix jacchus)

We tested current hypotheses on the functional organization of the third visual complex, a particularly controversial region of the primate extrastriate cortex. In anatomical experiments, injections of retrograde tracers were placed in the dorsal cortex immediately rostral to the second visual area (V2) of New World monkeys (Callithrix jacchus), revealing the topography of interconnections between the third tier cortex and the primary visual area (V1). The data indicate the presence of a dorsomedial area (DM), which represents the entire upper and lower quadrants of the visual field, and which receives strong, topographically organized projections from the superficial layers of V1. The visuotopic organization and boundaries of DM were confirmed by electrophysiological recordings in the same animals and by architectural characteristics which were distinct from those found in ventral extrastriate cortex rostral to V2. There was no electrophysiological or histological evidence for a transitional area between V2 and DM. In particular, the central representation of the upper quadrant in DM was directly adjacent to the representation of the horizontal meridian that marks the rostral border of V2. The present results argue in favor of the hypothesis that the third visual complex in New World monkeys contains different areas in its dorsal and ventral components: area DM, near the dorsal midline, and a homolog of area 19 of other mammals, located more lateral and ventrally. The characteristics of DM suggest that it may correspond to visual area 6 (V6) of Old World monkeys. (C) 2005 Wiley-Liss, Inc.