Neural coding of action in three dimensions: Task- and time-invariant reference frames for visuospatial and motor-related activity in parietal area V6A

Goal-directed movements involve a series of neural computations that compare the sensory representations of goal location and effector position, and transform these into motor commands. Neurons in posterior parietal cortex (PPC) control several effectors (e.g., eye, hand, foot) and encode goal location in a variety of spatial coordinate systems, including those anchored to gaze direction, and to the positions of the head, shoulder, or hand. However, there is little evidence on whether reference frames depend also on the effector and/or type of motor response. We addressed this issue in macaque PPC area V6A, where previous reports using a fixate-to-reach in depth task, from different starting arm positions, indicated that most units use mixed body/hand-centered coordinates. Here, we applied singular value decomposition and gradient analyses to characterize the reference frames in V6A while the animals, instead of arm reaching, performed a nonspatial motor response (hand lift). We found that most neurons used mixed body/hand coordinates, instead of \u201cpure\u201d body-, or hand-centered coordinates. During the task progress the effect of hand position on activity became stronger compared to target location. Activity consistent with body-centered coding was present only in a subset of neurons active early in the task. Applying the same analyses to a population of V6A neurons recorded during the fixate-to-reach task yielded similar results. These findings suggest that V6A neurons use consistent reference frames between spatial and nonspatial motor responses, a functional property that may allow the integration of spatial awareness and movement control

Magnification factors, receptive field images and point-image size in the superior colliculus of flying foxes: comparison with the primary visual cortex

The magnification factor (MF) of the stratum griseum superficialle (SGS) of the superior colliculus (SC) was calculated based on visual receptive fields recorded from anaesthetised and paralysed flying foxes (Pteropus spp.). In areal terms, the MF at the representation of central vision was 4-6 times larger than that in the peripheral representation. This variation is less marked than that observed in the primary visual area (VI), but is roughly that expected if the retinotopic map in the SC was defined by the distribution of ganglion cells in the retina. Two measures of the functional spread of activity in the SC, the receptive field images and the point-image size, were calculated. Receptive field images are remarkably similar throughout the SC. As in VI, the point-image size in the SGS of flying foxes is 0.5-0.6 mm and varies little with eccentricity. Bilateral ablation of the visual cortex results in a reduction of the mean receptive field size of neurones in the SGS, and the point-image size is reduced by half. However, the shape of the point-image function is not affected. These results demonstrate that the spread of activity in the SC is nearly constant throughout the retinotopic map and that this is primarily a result of the direct retinal projection. Although the visual cortex has an expanded central representation in comparison with the SC, the corticotectal pathway does not exert a preferential influence on the central representation of the SC

Visuotopic organisation of striate cortex in the marmoset monkey (Callithrix jacchus)

The visuotopic organisation of the primary visual cortex (V1) was studied by extracellular recordings in adult male marmosets (Callithrix jacchus) that were anaesthetised with sufentanil/nitrous oxide and paralysed with pancuronium bromide. Extensive sampling of the occipital region in four individuals and partial coverage of V1 in five others allowed not only the establishment of the normal visuotopy but also the study of interindividual variability. As in other primates, there was a single, continuous map of the contralateral hemifield in V1, with the upper visual quadrant represented ventrally and the lower quadrant represented dorsally. The surface area of V1, which was measured in two-dimensional reconstructions of the cortical surface, varied from 192 to 217 mm2. There was a marked emphasis on the representation of the foveal and parafoveal visual fields: the representation of the central 5 degrees of the visual field occupied 36-39% of the surface area of V1, whereas the central 10 degrees occupied 57-59%. No asymmetry between the representations of the upper and lower quadrants was apparent. The visual topography of V1 was highly consistent between individuals, relative to both sulcal landmarks and stereotaxic coordinates. The entire contralateral hemifield was represented in V1; in addition, neurones with receptive fields whose borders invaded the ipsilateral hemifield were observed within V1, less than 800 microns from the V1/V2 boundary. The total invasion of the ipsilateral hemifield was less than 0.5 degree at the centre of the fovea but reached 8 degrees at the periphery of the vertical meridian. Our results demonstrate that the organisation of V1 is similar in diurnal New and Old World simians, despite major variations in size, ecological niche, and timing of postnatal development across species

The occipitoparietal pathway of the macaque monkey: Comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas

The dendritic morphology of pyramidal cells located at the base of layer III in the primary visual area (V1), the second visual area (V2), the middle temporal area (MT), the ventral portion of the lateral intraparietal area (LIPv) and in the portion of cytoarchitectonic area 7a within the anterior bank of the superior temporal sulcus was revealed by injecting neurons with Lucifer Yellow in fixed, flattened slices of macaque monkey visual cortex. These areas correspond to different levels of the occipitoparietal cortical 'stream', which processes information related to motion and spatial relationships in the visual field. The tissue was immunocytochemically processed to obtain a light-stable diaminobenzidine reaction product, revealing the dendritic morphology in fine detail. Retrogradely labelled MT-projecting neurons in supragranular V1 (layer IIIc of Hassler's nomenclature, corresponding to Brodmann's layer IVb) were predominantly pyramidal, although many spiny multipolar (stellate) cells were also found. The average basal dendritic field area of pyramidal neurons in sublamina IIIc of V1 was significantly smaller than that in the homologous layer of V2, within the cytochrome oxidase-rich thick stripes. Furthermore, the average basal dendritic field areas of V1 and V2 pyramidal neurons were significantly smaller than those of neurons in MT, LIPv and area 7a. There was no difference in basal dendritic field area between layer III pyramidal neurons in areas MT, LIPv and 7a. While the shape of most basal dendritic fields was circularly symmetrical in the dimension tangential to the cortical layers, there were significant biases in complexity, with dendritic branches tending to cluster along particular axes. Sholl analysis revealed that the dendritic fields of neurons in areas MT, LIPv and 7a were significantly more complex (i.e. had a larger number of branches) than those of V1 or V2 neurons. Analysis of basal dendritic spine densities revealed regional variations along the dendrites, with peak densities being observed 40-130 microns from the cell body, depending on the visual area. The peak spine density of layer III pyramidal neurons in V1 was lower than that observed in V2, MT or LIPv, which were all similar. Pyramidal neurons in area 7a had the greatest peak spine density, which was on average 1.7 times that found in V1. Calculations based on the average spine density and number of dendritic branches at different distances from the cell body demonstrated a serial increase in the total number of basal dendritic spines per neuron at successive stations of the occipitoparietal pathway. Our observations, comparing dendritic fields of neurons in the homologous cortical layer at different levels of a physiologically defined 'stream', indicate changes in pyramidal cell morphology between functionally related areas. The relatively large, complex, spine-dense dendritic fields of layer III pyramidal cells in rostral areas of the occipitoparietal pathway allow these cells to sample a greater number of more diverse inputs in comparison with cells in 'lower' areas of the proposed hierarchy

Topography and extent of visual-field representation in the superior colliculus of the megachiropteran Pteropus

It has been proposed that flying foxes (genus Pteropus) have a primate-like pattern of representation in the superficial layers of the superior colliculus (SC), whereby the visual representation in this structure is limited by the same decussation line that limits the retino-geniculo-cortical projection (Pettigrew, 1986). To test this hypothesis, visual receptive fields were plotted based on single- and multi-unit recordings in the SC of ten flying foxes. A complete representation of the contralateral hemifi.eld was observed in the SC. Although the binocular hemifield of vision in Pteropus is 54 deg wide, receptive-field centers invaded the ipsilateral hemifield by only 8 deg, and the receptive-field borders by 13 deg. This invasion is similar to that observed at the border between visual areas VI and V2 in the occipital cortex. The extent of the ipsilateral invasion was not affected by a lesion that completely ablated the occipital visual areas, thus suggesting that this invasion may be consequence of a zone of nasotemporal overlap in the retinal projections to the two colliculi. Neurones located in the superficial layers typically responded briskly to stimulation of both eyes, with a bias towards the contralateral eye. After cortical lesions the neuronal responses to the ipsilateral eye were depressed, and the ocular-dominance histograms shifted towards an even stronger dominance by the contralateral eye. However, cells located in the rostral pole of the SC remained responsive to the ipsilateral eye after cortical lesions. Responses in the stratum opticum and stratum griseum intertrzediale were more severely affected by cortical lesions than those in the stratum griseum superficiale. Our results demonstrate that the SC in flying foxes retain some generalized mammalian characteristics, such as the stronger direct projections of the contralateral eye and the location of the upper, lower, central, and peripheral representations in the SC. Nonetheless, the extent of visual representation in the SC demonstrates a specialized, primate-like pattern. These observations are consistent with the hypothesis that megachiropterans are members of a group that branched off early during the differentiation of primates from basal mammals

The second visual area in the marmoset monkey: Visuotopic organisation, magnification factors, architectonical boundaries, and modularity

The organisation of the second visual area (V2) in marmoset monkeys was studied by means of extracellular recordings of responses to visual stimulation and examination of myelin- and cytochrome oxidase-stained sections. Area V2 forms a continuous cortical belt of variable width (1-2 mm adjacent to the foveal representation of V1, and 3-3.5 mm near the midline and on the tentorial surface) bordering V1 on the lateral, dorsal, medial, and tentorial surfaces of the occipital lobe. The total surface area of V2 is approximately 100 mm, or about 50% of the surface area of V1 in the same individuals. In each hemisphere, the receptive fields of V2 neurones cover the entire contralateral visual hemifield, forming an ordered visuotopic representation. As in other simians, the dorsal and ventral halves of V2 represent the lower and upper contralateral quadrants, respectively, with little invasion of the ipsilateral hemifield. The representation of the vertical meridian forms the caudal border of V2, with V1, whereas a field discontinuity approximately coincident with the horizontal meridian forms the rostral border of V2, with other visually responsive areas. The bridge of cortex connecting dorsal and ventral V2 contains neurones with receptive fields centred within 1°of the centre of the fovea. The visuotopy, size, shape and location of V2 show little variation among individuals. Analysis of cortical magnification factor (CMF) revealed that the V2 map of the visual field is highly anisotropic: for any given eccentricity, the CMF is approximately twice as large in the dimension parallel to the V1/V2 border as it is perpendicular to this border. Moreover, comparison of V2 and V1 in the same individuals demonstrated that the representation of the central visual field is emphasised in V2, relative to V1. Approximately half of the surface area of V2 is dedicated to the representation of the central 5°of the visual field. Calculations based on the CMF, receptive field scatter, and receptive field size revealed that the point-image size measured parallel to the V1/V2 border (2-3 mm) equals the width of a full cycle of cytochrome oxidase stripes in V2, suggesting a close correspondence between physiological and anatomical estimates of the dimensions of modular components in this area

Organization of the second visual area in the megachiropteran bat pteropus

The organization of peristriate cortex was studied in nine flying foxes (genus Pteropus). Based on receptive field mapping and architectonic data, we reported on the organization of the second visual area (V2). V2 forms a continuous belt 2-4 mm wide bordering V1 anteriorty. In each hemisphere, V2 contains a precisely organized representation of the entire contralateral visual field. The vertical meridian of the visual field (VM), and a short strip of the ipsilateral hemifield are represented at the posterior border of V2, with V1. The area centralis is represented approximately at the center of the posterior border of V2. At each mediolateral level, progressively more peripheral portions of the visual field are represented as V2 is crossed from posterior to anterior. The representation of the upper quadrant is continuous, and confined to the lateral half of V2. In contrast, the representation of the lower quadrant is split along a line running from the temporal edge of the field of vision to the optic disk. As a result of this arrangement, the portions of the lower quadrant close to the VM are represented medially, and those away from the VM laterally in V2. The entire representation of the horizontal meridian is located in lateral V2, and is not split between medial and lateral V2 as in primates. The linear cortical magnification factor (CMF) decays by a factor of 3-5 from the central to the peripheral repre-sentation. The CMF is anisotropic, and equal distances in the visual field are magnified twice as much parallel to the V1/V2 border than perpendicular to this border. Moreover, points in the lower quadrant are magnified relative to symmetrical points in the upper quadrant. V2 is histologically distinct from all surrounding areas in both cytochrome oxidase- and Nissl-stained sections. These results suggest that V2 is an homologous area common to all archontans, and imply that much of the variability reported among mammals may be due to technical factors, rather than true species differences