The morphology of the koniocellular axon pathway in the macaque monkey

The key objective of this study was to determine the distribution and morphology of koniocellular (K) lateral geniculate nucleus (LGN) axons in primary visual cortex (V1) of the macaque monkey. In particular, we were interested in understanding whether subpopulations of K axons exist in this species and, if so, if these subpopulations arise from different K layers of the LGN. Restricted injections of the tracers, biotinilated dextran amine, or Phaseolus vulgaris leucoagglutinin were targeted to specific LGN K layers under electrophysiological guidance and immunocytochemistry was used to visualize labeled axons in cortex that were subsequently reconstructed through serial sections. A total of 36 complete axons and 166 axon segments were reconstructed. Our results identified at least 2 main subpopulations of K axons in macaque V1 based on branching patterns and bouton distribution. Axons that arise primarily from LGN layers K1 and K2 are morphologically simple and tend to branch in cortical layers 1 and 3A. These axons give rise to fewer boutons than seen in axons arising from the dorsal K LGN layers K3-K6. Axons that arise from LGN layers K3-K6 terminate as complex, focused arbors in the cytochrome oxidase (CO) blobs in layer 3Balpha, with only occasional simple projections to the more superficial layers of cortex. Combined with previous observations, our data suggest that there are at least 3 subclasses of K LGN axons in macaque monkey that are similar to K axons identified earlier in both nocturnal simian owl monkeys (Ding and Casagrande 1997) and in prosimian, bush babies (Lachica and Casagrande 1992) suggesting that the LGN K channels that terminate in the CO blobs and in layer 1 are not unique to macaque monkeys but are a common primate feature.     

Differential architecture of multisynaptic geniculo-cortical pathways to V4 and MT

Parallel visual pathways in the primate brain known as the dorsal and ventral streams receive retinal inputs mainly through the magnocellular (M) and parvocellular (P) layers of the lateral geniculate nucleus. Inputs from these layers terminate within distinct parts of layer 4C of V1 (visual area 1). Due to the complexity of M- and P-derived neural connectivity in V1 and higher visual areas, the contributions of M and P inputs to the dorsal and ventral streams remain unclear. Employing retrograde transsynaptic transport of rabies virus, we analyzed the architecture of bottom-up pathways toward ventral stream area V4 (visual area 4) and dorsal stream area MT (middle temporal area). We found that V4 receives both M and P inputs "trisynaptically" from layer 4C via layer 2/3 of V1, whereas MT receives M-dominant input "disynaptically" from layer 4C via layer 4B of V1. V4 also receives disynaptic input from the dorsal stream portion of V2 (visual area 2) (i.e., cytochrome oxidase-stained thick stripes). Moreover, both M and P inputs reach V4 trisynaptically and MT disynaptically through "short-cut" pathways that bypass layer 4C of V1. The differential patterns of multisynaptic geniculo-cortical pathways to V4 and MT imply distinct modes of information processing in the dorsal and ventral streams.     

Quantitative analysis of the corticocortical projections to the middle temporal area in the marmoset monkey: evolutionary and functional implications

The connections of the middle temporal area (MT) were investigated in the marmoset, one of the smallest primates. Reflecting the predictions of studies that modeled cortical allometric growth and development, we found that in adult marmosets MT is connected to a more extensive network of cortical areas than in larger primates, including consistent connections with retrosplenial, cingulate, and parahippocampal areas and more widespread connections with temporal, frontal, and parietal areas. Quantitative analyses reveal that MT receives the majority of its afferents from other motion-sensitive areas in the temporal lobe and from the occipitoparietal transition areas, each of these regions containing approximately 30% of the projecting cells. Projections from the primary visual area (V1) and the second visual area (V2) account for approximately 20% of projecting neurons, whereas "ventral stream" and higher-order association areas form quantitatively minor projections. A relationship exists between the percentage of supragranular layer neurons forming the projections from different areas and their putative hierarchical rank. However, this relationship is clearer for projections from ventral stream areas than it is for projections from dorsal stream or frontal areas. These results provide the first quantitative data on the connections of MT and extend current understanding of the relationship between cortical anatomy and function in evolution.     

Development of Forward and Feedback Connections between Areas V1 and V2 of Human Visual Cortex

We have determined the sequence in which forward connectionsbetween visual cortical areas V1 and V2, and feedback connectionsbetween V2 and V1 develop in humans. For this purpose Dii wasinjected into V1 and V2 of postmortem brains of different pre-and postnatal ages. The laminar distribution of labeled fibersand cell bodies In V1 and V2 Indicates that forward and feedbackconnections emerge shortly before birth. The development ofboth pathways proceeds over several postnatal months such thatthe laminar termination pat tern of forward connections appearsrelatively mature before feedback connections reach their matureform. At 31 weeks of gestation both forward and feedback connectionsoriginate exclusively from deep-layer neu rons, which extendaxons in deep layers only. By 9 d postnatal, forward connectionsfrom V1 to V2, n ad dition to layers 5 and 6, also arise fromneurons in layer 4B of V1. At this stage for the first timeforward fibers enter layer 4 at the topographically appropriatelocation of V2. At 9 d postnatal most feedback fibers from V2still occupy deep layers of Vi but many, through inter stitialgrowth, elaborate vertical sprouts at regular in tervals alongthe length of horizontal axons. As feedback connections mature,distal segments of horizontal axons are pruned beck to branchpoints and fibers assume L-shaped configurations. By 1 weeksof age forward fibers from V1 enter V2 through deep and superficiallayers and provide input to layers 3 and 4. At this stage feedbackfibers from V2 have entered layer 4B of V1. By 4 months of ageforward connections have assumed all the laminar characteristicsof mature connections; that is, they arise from layers 2/3,48, 5, and 6 of V1, and terminate In layers 3 and 4 of V2. Insharp contrast, at 4 months of age feedback connections to V1are still immature, showing terminations In layers 4B, 5, and6 but no input to layer 2/3. The protracted postnatal emergence of feedback con nectionsis similar to that of local long-range connec tions within layer2/3 of V1 (Burkhalter at al., i993). Since both of thsse circuitsare thought to provide in formation about the context in whichobjects are seen, it is interesting to speculate that the lateonset of texture segmentation in infants (Atkinson and Braddick.1992; Sireteanu and Rieth, 1992) may be related to the postnatal maturation of specific Intracortical circuits.     

Differential expression patterns of striate cortex-enriched genes among Old World, New World, and prosimian primates

A group of 5 genes, OCC1, testican-1, testican-2, 5-HT1B, and 5-HT2A, are selectively expressed in layer 4 (4C of Brodmann) of striate cortex (visual area V1) of both Old World macaques and New World marmoset monkeys. The expression of these genes is activity dependent, as expression is reduced after blocking retinal activity. Surprisingly, the pronounced expression pattern has not been found in rodents or carnivores. Thus, these genes may be highly expressed in V1 of some but perhaps not all primates. Here, we compared the gene expression in members of 3 major branches of primate evolution: prosimians, New World monkeys, and Old World monkeys. Although the expression pattern of 5-HT1B was well conserved, those of the other genes varied from the least distinct in prosimian galagos to successively more in New World owl monkeys, marmosets, squirrel monkeys, and Old World macaque monkeys. In owl monkeys, the expression of 5-HT2A was significantly reduced by monocular tetrodotoxin injection, while those of OCC1 and 5-HT1B were not. Thus, we propose that early primates had low levels of expression and higher levels emerged with anthropoid primates and became further enhanced in the Old World catarrhine monkeys that are more closely related to humans.     

Anatomical evidence for classical and extra-classical receptive field completion across the discontinuous horizontal meridian representation of primate area V2

In primates, a split of the horizontal meridian (HM) representation at the V2 rostral border divides this area into dorsal (V2d) and ventral (V2v) halves (representing lower and upper visual quadrants, respectively), causing retinotopically neighboring loci across the HM to be distant within V2. How is perceptual continuity maintained across this discontinuous HM representation? Injections of neuroanatomical tracers in marmoset V2d demonstrated that cells near the V2d rostral border can maintain retinotopic continuity within their classical and extra-classical receptive field (RF), by making both local and long-range intra- and interareal connections with ventral cortex representing the upper visual quadrant. V2d neurons located <0.9-1.3 mm from the V2d rostral border, whose RFs presumably do not cross the HM, make nonretinotopic horizontal connections with V2v neurons in the supra- and infragranular layers. V2d neurons located <0.6-0.9 mm from the border, whose RFs presumably cross the HM, in addition make retinotopic local connections with V2v neurons in layer 4. V2d neurons also make interareal connections with upper visual field regions of extrastriate cortex, but not of MT or MTc outside the foveal representation. Labeled connections in ventral cortex appear to represent the "missing" portion of the connectional fields in V2d across the HM. We conclude that connections between dorsal and ventral cortex can create visual field continuity within a second-order discontinuous visual topography.     

Neurons in V1 patch columns project to V2 thin stripes

In the primate, connections between primary visual cortex (V1) and the second visual area (V2) are segregated according to the characteristic pattern of cytochrome oxidase (CO) activity in each of these cortical areas. Patches supply thin stripes, whereas interpatches supply pale stripes and thick stripes. Previously, the projection from patches to thin stripes was reported to arise exclusively from layer 2/3. In this present report, we made injections of a retrograde tracer, cholera toxin-B (CTB-Au), into macaque V2 thin stripes to re-examine the laminar origin of their input from V1. While the great majority of cells indeed resided in layer 2/3, small populations were also present in layers 4A, 4B, and 5/6. The location of CTB-filled cells in each layer was analyzed to determine the relationship with CO patches. Cells in layers 2/3, 4A, and 4B were aggregated into patches, forming columns that project to thin stripes. Surprisingly, cells in layer 5/6 were scattered, seemingly at random. These findings confirm that the main V1 projection to V2 stripes emanates from patches in layer 2/3. However, multiple V1 layers innervate V2 thin stripes, and the projection from layer 5/6 does not respect the patch/interpatch dichotomy.     

Laminar patterns of local excitatory input to layer 5 neurons in macaque primary visual cortex

Layer 5 neurons in primary visual cortex make putative reciprocal feedback connections to the superficial layers. To test this hypothesis, we employed scanning laser photostimulation combined with intracellular dye injection to examine local functional excitatory inputs to and axonal projections from individual layer 5 neurons in brain slices from monkey V1. In contrast with previous studies of other V1 neurons, layer 5 neurons received significant input from nearly all of the cortical layers, suggesting individual layer 5 cells integrate information from a broad range of input sources. Nevertheless relative strengths of laminar inputs varied across neurons. Cluster analysis of relative strength of laminar inputs to individual layer 5 neurons revealed four discrete clusters representing recurring input patterns; each cluster included both excitatory and inhibitory neurons. Twenty-five of 40 layer 5 neurons fell into two clusters, both characterized by very strong input from superficial layers. These input patterns are consistent with layer 5 neurons providing feedback to superficial layers. The remaining 15 neurons received stronger input from deep layers. Differences in input from layer 4Calpha versus 4Cbeta also suggest specific associations of the magnocellular and parvocellular visual pathways, with populations receiving stronger input from deep versus superficial cortical layers.     

The distribution of NADPH diaphorase and nitric oxide synthetase (NOS) in relation to the functional compartments of areas V1 and V2 of primate visual cortex

The primary visual cortex (V1) of primates receives visual signals from cells in the koniocellular (K), magnocellular (M) and parvocellular (P) layers of the lateral geniculate nucleus (LGN). The functional role of the K pathway is unknown, but one proposal is that it modulates visual activity locally via release of nitric oxide (NO). One goal of this study was to examine the distribution of nitric oxide synthetase (NOS), the enzyme that produces NO, using immunocytochemistry for brain NOS (bNOS) or histochemistry for nicotinamide adenine dinucleotide phosphate (NADPH) diaphorase activity in the V1 target cells of the K pathway and within the LGN itself. A second goal was to examine bNOS and NADPH diaphorase activity within proposed functional compartments in the second visual area (V2). We examined the LGN, V1 and V2 in squirrel monkeys, owl monkeys and bushbabies. In V1 and V2, we found that dense neuropil staining for NADPH diaphorase mirrored the pattern of high metabolic activity shown with cytochrome oxidase (CO) staining but did not necessarily mirror the pattern of immunolabeling seen with antibodies against NOS. The smooth stellate cells stained for NADPH diaphorase or bNOS were sparse and did not colocalize with LGN recipient zones in V1 or with the CO compartments in V2. LGN cells projecting to V1, including K, M and P cells, were negative for bNOS and NADPH diaphorase. Therefore, high levels of NOS are not limited to the K pathway. Instead, dense NOS activity is present in interneurons and within the neuropil of V1 and V2 that exhibit high metabolic demand.     

Configuration, in serial reconstruction, of individual axons projecting from area V2 to V4 in the macaque monkey.

The detailed morphology of long extrinsically projecting axons in the neocortex has been difficult to investigate and is in fact poorly understood. Some data, based on extracellular injections of Phaseolus vulgaris leucoagglutinin (PHA-L), are available for individual axons projecting from area V1 to area V2 or MT. Like geniculocortical projections, axons projecting from area V1 to area MT are readily identifiable (they typically have a bistratified termination pattern and large terminal specializations and are of large caliber), but those projecting from area V1 to V2 are more variable. To provide a broader basis for interpreting constant and variable features of axon morphology, we used high-resolution serial section reconstruction to analyze small populations of PHA-L-labeled axons projecting from area V2 to V4. Reconstruction of 20 axons suggests that this system is variable in terms of overall configuration and laminar distribution. Most terminal arbors are located at the border between layers 3 and 4, but some remain entirely within layer 3 or 4, some target preferentially the superficial layers (1, 2, and 3A), and some have collaterals in layer 5 or, rarely, layer 6. Arbor size is fairly constant among the three visual cortical projections examined so far (typically about 200 microns in diameter). In area V4, however, axons frequently have three or four separate arbors, which branch divergently (in one instance, over 2.6 mm x 3.0 mm). These features may be correlated with aspects of the particular functional organization of area V4, such as coarse topography, large receptive field size, and modularity. Axonal variability may also denote differences, morphological or physiological, among neurons of origin in area V2.     

Eye-hand coordination during reaching. I. Anatomical relationships between parietal and frontal cortex

The anatomical and physiological substrata of eye-hand coordination during reaching were studied through combined anatomical and physiological techniques. The association connections of parietal areas V6A and PEc, and those of dorso-rostral (F7) and dorso-caudal (F2) premotor cortex were studied in monkeys, after physiological characterization of the parietal regions where retrograde tracers were injected. The results show that parieto-occipital area V6A is reciprocally connected with F7, and receives a smaller projection from F2. Local parietal projections to V6A arise from areas MIP and, to a lesser extent, 7m, PEa and PEC: On the contrary, parietal area PEc is strongly and reciprocally connected with the part of F2 located close to the pre-central dimple (pre-CD). Local parietal projections to PEc come from a distributed network, including PEa, MIP, PEci and, to a lesser extent, 7m, V6A, 7a and MST. Premotor area F7 receives parietal projections mainly from 7m and V6A, and local frontal projections mainly from F2. On the contrary, premotor area F2 in the pre-CD zone receives parietal inputs from PEc and, to a lesser extent, PEci, while in the peri-arcuate zone F2 receives parietal projections from PEa and MIP. Local frontal projections to F2 pre-CD mostly stem from F4, and, to a lesser extent, from F7 and F3, and CMAd; those addressed to peri-arcuate zone of F2 arise mainly from F5 and, to a lesser extent, from F7, F4, dorsal (CMAd) and ventral (CMAv) cingulate motor areas, pre-supplementary (F6) and supplementary (F3) motor areas. The distribution of association cells in both frontal and parietal cortex was characterized through a spectral analysis that revealed an arrangement of these cells in the form of bands, composed of cell clusters, or 'columns'. The reciprocal connections linking parietal and frontal cortex might explain the presence of visually related and eye-position signals in premotor cortex, as well as the influence of information about arm position and movement direction in V6A and PEC: The association connections identified in this study might carry sensory as well motor information that presumably provides a basis for a re-entrant signaling. This might be necessary to match retinal-, eye- and hand-related information underlying eye-hand coordination during reaching.     

Laminar distribution of neurons projecting from area V1 to V2 in macaque and squirrel monkeys.

The present study reevaluates the sublaminar distribution and cellular morphology of neurons projecting from area V1 to V2. Observations are based on retrogradely transported HRP, Phaseolus vulgaris leucoagglutinin (PHA-L), or biocytin after injections made in area V2 of three squirrel monkeys and eight macaques. With material prepared in the coronal or horizontal tissue planes, it is clear that projection neurons in V1, in both species, are concentrated in layer 4B and in a single band (150-250 microns wide) restricted to the upper subdivision of layer 3 (layer 3A). There are also labeled neurons, but fewer in number, in layers 3B and 4A, and occasionally in layers 2 and 5. Golgi-like labeling from PHA-L or biocytin confirmed that most of the projection neurons in layer 3A are pyramidal. As reported for several other corticocortical systems, these pyramidal neurons differ in soma size, soma shape, and dendritic geometry. These results emphasize the complex organization of layer 3, and the distributed nature of efferent projections from area V1. Given the selective connectivity of vertical interlaminar networks, these results specifically suggest that information transmitted to area V2 from neurons in layer 3A reflects more highly processed, convergent input than that originating from either layer 3B or 4B.     

Organization of horizontal axons in the inferior temporal cortex and primary visual cortex of the macaque monkey

We investigated the organization of horizontal connections at two distinct hierarchical levels in the ventral visual cortical pathway of the monkey, the inferior temporal (TE) and primary visual (V1) cortices. After injections of anterograde tracers into layers 2 and 3, clusters of terminals ('patches') of labeled horizontal collaterals in TE appeared at various distances up to 8 mm from the injection site, while in V1 clear patches were distributed only within 2 mm. The size and spacing of these patches in TE were larger and more irregular than those observed in V1. The labeling intensity of patches in V1 declined sharply with distance from the injection site. This tendency was less obvious in TE; a number of densely labeled patches existed at distant sites beyond weakly labeled patches. While injections into both areas resulted in an elongated pattern of patches, the anisotropy was greater in TE than in V1 for injections of a similar size. Dual tracer injections and larger-sized injections further revealed that the adjacent sites in TE had spatially distinct horizontal projections, compared to those in V1. These area-specific characteristics of the horizontal connections may contribute to the differences in visual information processing of TE and V1.     

Connections of Inferior Temporal Areas TEO and TE with Parietal and Frontal Cortex in Macaque Monkeys

Inferior temporal cortex is perhaps the highest visual processingarea and much anatomical work has focused on its connectionswith other visual areas in temporal and occipital cortex. Herewe report connections of inferior temporal cortex with regionsin the frontal and parietal lobes. Inferior temporal areas TEOand TE were injected with WGA-HRP and ³H-AA, respectively, orvice versa, in 1-week-old infant and 3–4–year-oldadult monkeys (Macaca mulatta). The results indicated that whereasTEO has more extensive connections with parietal areas, TE hasmore extensive connections with prefrontal areas. Thus, in theintraparietal sulcus, area TEO is connected with areas LIPd,LIPv, and V3A, and with the as yet undefined region betweenLIPv and V3A, whereas the connections of TE are predominantlywith LIPd, and to a lesser extent with LIPv. In the prefrontalcortex, area TE is connected with areas 8 and 45 in the inferiorlimb of the anterior bank of the arcuate sulcus, with area 12on the inferior prefrontal convexity, and with areas 11 and13 on the orbital surface. By contrast, the connections of areaTEO are limited to areas 8, 45, and 12. Furthermore, withinprefrontal cortex, the projections from areas TEO and TE terminatein different layers in areas 8 and 45, such that those fromTEO terminate in all layers, whereas those from TE terminatein layers I and V/VI only. In contrast to the connections ofareas TEO and TE with various medical temporal-lobe and subcorticalstructures, which are immature in infant monkeys (Webster etal., 1991, 1993b), the connections with parietal and prefrontalareas appear adult-like as early as 1 week of age.     

Direct Temporal-Occipital Feedback Connections to Striate Cortex (V1) in the Macaque Monkey

Although there have been reports of sparse projections fromtemporal areas TE, TF, and even TH to area V1, it is generallybelieved that cortical afferents to V1 originate exclusivelyfrom prestriate areas. Injections of anterograde tracers inanterior occipital and temporal areas, however, consistentlyproduce labeled terminals in area V1. In order to confirm theseresults and display the full range of foci projecting to V1,we injected V1 in two monkeys with the retrograde tracer fastblue. Feedback connections were found, as expected, from severalprestriate areas (V2, V3, V4, and MT). These originate fromneurons in layers 3A and 6. Connections were also found fromseveral more distal regions, namely, areas TEO, TE, TF, TH,and from cortex in the occipitotemporal and superior temporal(STS) sulci. Filled neurons occurred in two small foci in thecaudal intraparietal sulcus. These more distal feedback connectionstend to originate only from layer 6. An additional injectionof the retrograde tracer diamidino yellow in area V2 of oneanimal revealed a similarly widespread network of feedback connections.In some areas (In the STS and in TEO), 10–15% of fluorescentneurons were double-labeled. These results indicate that feedback connections to early visualcortex derive from a widespread network of areas, includinglimbic-associated cortices. These connectional patterns testifyto the massive recursiveness of anatomical pathways. As thereare no reports of projections from V1 to anterior temporal cortices,our results also indicate that some cortical feedback connectionsmay not be strictly reciprocal.     

Cortical connections of area V4 in the macaque

To determine the locus, full extent, and topographic organization of cortical connections of area V4 (visual area 4), we injected anterograde and retrograde tracers under electrophysiological guidance into 21 sites in 9 macaques. Injection sites included representations ranging from central to far peripheral eccentricities in the upper and lower fields. Our results indicated that all parts of V4 are connected with occipital areas V2 (visual area 2), V3 (visual area 3), and V3A (visual complex V3, part A), superior temporal areas V4t (V4 transition zone), MT (medial temporal area), and FST (fundus of the superior temporal sulcus [STS] area), inferior temporal areas TEO (cytoarchitectonic area TEO in posterior inferior temporal cortex) and TE (cytoarchitectonic area TE in anterior temporal cortex), and the frontal eye field (FEF). By contrast, mainly peripheral field representations of V4 are connected with occipitoparietal areas DP (dorsal prelunate area), VIP (ventral intraparietal area), LIP (lateral intraparietal area), PIP (posterior intraparietal area), parieto-occipital area, and MST (medial STS area), and parahippocampal area TF (cytoarchitectonic area TF on the parahippocampal gyrus). Based on the distribution of labeled cells and terminals, projections from V4 to V2 and V3 are feedback, those to V3A, V4t, MT, DP, VIP, PIP, and FEF are the intermediate type, and those to FST, MST, LIP, TEO, TE, and TF are feedforward. Peripheral field projections from V4 to parietal areas could provide a direct route for rapid activation of circuits serving spatial vision and spatial attention. By contrast, the predominance of central field projections from V4 to inferior temporal areas is consistent with the need for detailed form analysis for object vision.     

Patterns of Connectivity in the Neocortex of the Echidna (Tachyglossus aculeatus)

Patchy connections were traced in the visual and auditory cortexof the echidna (Tachyglossus aculeatus). Labeled neurons andclusters of axon collaterals were distributed in regular arraysafter the application of a small crystal (100–300 µmdiameter) of the carbocyanine dye Dil (1,1'-dioctadecyl-3,3,3',3'-tetramethylindocart)ocyaninepar-chlorate) into the upper cortical layers. In general, theanterograde and retrograde labels were in register, but whereasthe anterograde label was distributed throughout all six layers,the retrogradely filled neurons were absent from layer 1 andthe highest density of labeled cells was in layers 5 and 6.The cells contained within the patches were all pyramidal orpyramid-like and contained long spines on their dendrites. Therefore,despite their unusual location within the lateral posteriorcortex, the internal structure of the echidna visual and auditorycortices resembled that of eutherian mammals in containing aregular columnar array of connections that may represent thecorti-cocortical projections.     

The Functional Organization of Local Circuits in Visual Cortex: Insights from the Study of Tree Shrew Striate Cortex

We have used a combination of anatomical and physiological techniquesto explore the functional organization of vertical and horizontalconnections in tree shrew striate cortex. Our studies of verticalconnections reveal a remarkable specificity in the laminar arrangementof the projections from layer IV to layer III that establishesthree parallel intracortical pathways. The pathways that emergefrom layer IV are not simple continuations of parallel thalamocorticalpathways. Layer IV and its connections with layer II/III restructurethe inputs from the LGN, combining the activity from ON andOFF channels and from the left and right eye and transmit theproducts of this synthesis to separate strata within the overlyinglayers. In addition, studies of two other prominent verticalconnection pathways, the projections from layer VI to layerIV and from layer II/III to layer V suggest that the parallelnature of these systems is perpetuated throughout the corticaldepth. Our studies of horizontal connections have revealed a systematicrelationship between a neuron's orientation preference and thedistribution of its axon arbor across the cortical map of visualspace. Horizontal connections in layer II/III extend for greaterdistances and give rise to a greater number of terminals alongan axis of the visual field map that corresponds to the neuron'spreferred orientation. These findings suggest that the contributionof horizontal inputs to the response properties of layer II/IIIneurons is likely to be greater in regions of visual space thatlie along the axis of preferred orientation (endzones) thanalong the orthogonal axis (side zones). Topographically alignedhorizontal connections may contribute to the orientation preferenceof layer II/III neurons and could account for the axial specificityof some receptive field surround effects. Together, these results emphasize that specificity in the spatialarrangement of local circuit axon arbors plays an importantrole in shaping the response properties of neurons in visualcortex.     

Laminar development of receptive fields,maps and columns in visual cortex: the coordinating role of the subplate

How is development of cortical maps in V1 coordinated across cortical layers to form cortical columns? Previous neural models propose how maps of orientation (OR), ocular dominance (OD), and related properties develop in V1. These models show how spontaneous activity, before eye opening, combined with correlation learning and competition, can generate maps similar to those found in vivo. These models have not discussed laminar architecture or how cells develop and coordinate their connections across cortical layers. This is an important problem since anatomical evidence shows that clusters of horizontal connections form, between iso-oriented regions, in layer 2/3 before being innervated by layer 4 afferents. How are orientations in different layers aligned before these connections form? Anatomical evidence demonstrates that thalamic afferents wait in the subplate for weeks before innervating layer 4. Other evidence shows that ablation of the cortical subplate interferes with the development of OR and OD columns. The model proposes how the subplate develops OR and OD maps, which then entrain and coordinate the development of maps in other lamina. The model demonstrates how these maps may develop in layer 4 by using a known transient subplate-to-layer 4 circuit as a teacher. The model subplate also guides the early clustering of horizontal connections in layer 2/3, and the formation of the interlaminar circuitry that forms cortical columns. It is shown how layer 6 develops and helps to stabilize the network when the subplate atrophies. Finally the model clarifies how brain-derived neurotrophic factor (BDNF) manipulations may influence cortical development.     

A neural model of how horizontal and interlaminar connections of visual cortex develop into adult circuits that carry out perceptual grouping and learning

A neural model suggests how horizontal and interlaminar connections in visual cortical areas V1 and V2 develop within a laminar cortical architecture and give rise to adult visual percepts. The model suggests how mechanisms that control cortical development in the infant lead to properties of adult cortical anatomy, neurophysiology and visual perception. The model clarifies how excitatory and inhibitory connections can develop stably by maintaining a balance between excitation and inhibition. The growth of long-range excitatory horizontal connections between layer 2/3 pyramidal cells is balanced against that of short-range disynaptic interneuronal connections. The growth of excitatory on-center connections from layer 6-to-4 is balanced against that of inhibitory interneuronal off-surround connections. These balanced connections interact via intracortical and intercortical feedback to realize properties of perceptual grouping, attention and perceptual learning in the adult, and help to explain the observed variability in the number and temporal distribution of spikes emitted by cortical neurons. The model replicates cortical point spread functions and psychophysical data on the strength of real and illusory contours. The on-center, off-surround layer 6-to-4 circuit enables top-down attentional signals from area V2 to modulate, or attentionally prime, layer 4 cells in area V1 without fully activating them. This modulatory circuit also enables adult perceptual learning within cortical area V1 and V2 to proceed in a stable way.