We used horseradish peroxidase (HRP) to orthogradely label afferent axons in macaque striate cortex. Of the 38 axons that we recovered, nine were recorded intracelhrlarly before being filled with HRP. Light microscope and computer reconstructions of filled processes reveal highly stereotyped patterns of arborization and suggest that there are at least five discrete populations of lateral geniculate nucleus (LGN) afferent axon: (1) those to layer 4Cp, which have extremely circumscribed, dense terminal fields (small branches of which occasionally intrude into 4Ca) but which have not been shown to project to other laminae; (2) afferents to layer 4A, which in some cases send fine ascending collaterals into layer 2-3 and which do not, apparently, send collaterals to other laminae; (3) afferents to layer 1, which are fine, extend over large distances horizontally, and send collaterals to layer 6A; (4) afferents to the lower two-thirds of layer 4Ca, which have few or no collaterals in layer 6; and (5) afferents to the upper half of layer 4Ca, which have arborizing collaterals in layer 6B. Of the nine axons that were recorded intracellularly, those with projections to layer 4Cp (two axons) and to layer 1 (one axon) had color-selective properties, whereas those (six axons) which arborized in 4Ca all had transient, broad band and highly contrast-sensitive receptive fields. These properties are consistent with derivations from somata in the parvocellular and magnocellular divisions of the LGN, respectively. Afferents to 4Ca were found to cover approximately 6 times as much surface area as afferents to 4Cp. The preterminal trunks of all axons were found to follow tortuous paths through the neuropil-paths that may derive from axon segregation during development. The wide ranging, patchy distributions of single afferents in 4C~u suggest that individual 4& axons supply more than one ocular dominance stripe. In one case where the terminal arborization of a 4Ca axon was mapped against the transneuronally determined pattern of ocular dominance, three separate patches of terminal boutons were indeed found to coincide with the bands of one eye.The primate visual system is characterized by successive and discrete transformations in the neural representation of visual space. One such transformation occurs between the lateral geniculate nucleus (LGN) and cells in the thalamo-recipient laminae of striate cortex. Even though the receptive fields of cells in layer 4C-the layer that receives most of the LGN input-lack orientation selectivity and to some extent resemble those of the LGN, the transfer of information seems not to occur in

We have studied the intrinsic organization of macaque striate cortex by tracing the pattern of horseradish peroxidase (HFiP)-labeled axons and cell bodies produced by microinjections of HRP into single cortical laminae. Both anterograde and retrograde transport results were used to examine: (1) the pattern of projections from lamina 4C to the superficial layers; (2) the projection from lamina 4C to deeper cortical layers; and (3) the projections to lamina 4C from other cortical laminae.Laminae 4C0 and 4Cfi differ in their pattern of projections to the superficial layers of striate cortex. Axons from neurons in lamina 4C/3 ascend through lamina 48 without giving off collaterals and terminate in lamina 4A and in the base of lamina 3. By contrast, axons from neurons in lamina 4Ccu terminate in lamina 48 and less densely in the 4A/3B region.The projection from lamina 4Cp to lamina 4A is particularly dense and is distributed in a patchy fashion immediately above each injection site. The projection from lamina 4Cp to lamina 38 appears less dense and more widespread; we estimate that individual 4Cj3 axons may spread laterally for more than 400 pm. Furthermore, the pattern of HRP-labeled cell bodies in lamina 4Cj3 following injections into laminae 4A and 3B provides evidence for a subdivision within SC& These injections always produce a large number of labeled neurons in the upper part of lamina 4C& whereas the lower portion contains few labeled neurons that are located immediately under the center of the injection site.Both lamina 4& and lamina 4Cp also contribute less dense projections to the deeper layers of cortex. Lamina 4Cj3 projects mainly to lamina 6, whereas lamina 4Ca contributes axon terminals to both lamina 5A and lamina 6.Neurons in lamina 6 provide the bulk of the intracortical projections to lamina 4C. These results confirm or refine many conclusions about intrinsic connections of striate cortex drawn from Golgi material and suggest new patterns of connections not suspected from previous work.The key to understanding cortical function lies in establishing the way in which inputs from the thalamus and other brainstem regions are transformed into the response properties of output neurons. Although we are still far from understanding the nature of this complex process, it is clear that the achievement of this objective will require a detailed knowledge of intracortical circuitry and the relation of this circuitry to afferent and efferent cell groups.The macaque striate cortex provides an excellent system for the study of intracortical circuitry because of the remarkable degree of lamlnar segregation of different afferent and efferent pathways. For example, inputs from the magnocellular and parvocellular laminae of the lateral geniculate nucleus (LGN) terminate in separate and largely nonoverlaping tiers within lamina 4C with magnocellular afferents occupying a more superficial position (lamina 4Ca) than parvocellular ones (lamina 4Cp) (Hubel and Wiesel, 1972; Hendrickson et al., 1978). Likewise, the...

The directional preference of neurons sampled from all layers of the striate cortex was determined using the responses to drifting grating stimuli of optimal spatial and temporal frequency. In addition, contrast sensitivity as a function of spatial frequency was measured and from the resulting spatial contrast sensitivity function the peak contrast sensitivity and optimal spatial frequency were obtained. The distribution of directionally selective cells showed a distinct laminar pattern. Upper layer 4 (4a, 4b, and 4c alpha) and layer 6 were the only cortical layers with neurons that showed a pronounced preference for the direction of stimulus motion. The directionally selective cells in these layers are among those with the highest contrast sensitivities but had optimal spatial frequencies that were confined to the low and middle range of the optimal spatial frequency distribution. These findings suggest that the directionally selective cells may fall into at least 2 distinct populations, which may be the first stages in the visual pathway that correspond to those channels, inferred from psychophysical experiments, that underlie the detection of movement.

We have exploited a technique for making small injections of horseradish peroxidase into single cortical laminae in order to study axonal projections in macaque striate cortex. In the preceding paper (Fitzpatrick, D., J. S. Lund, and G. G. Blasdel (1985) J. Neurosci. 5: 3329-3349) we examined the projections of cells in lamina 4C--cells that receive most of their input from the lateral geniculate nucleus. The present paper deals with the projections of neurons that lie outside of lamina 4C. Among our findings are several projections that previously had not been described in the monkey. These include: a strong and precise (point-to-point) projection from lamina 4B to lamina 2/3A, a reciprocal projection from 2/3A back to 4B, a definite projection from lamina 4B to 5B, as well as a prominent input to lamina 6 from 5B. In many cases, we find it possible to trace the flow of visual information through several "circuits" in striate cortex that have, as their output, projections to extrastriate cortex or to the brainstem. Our results offer additional insights in this regard since we are able, in many cases, to compare the lateral spreads of particular projections. These vary and can be separated into at least three categories: those that terminate in a precise, point-to-point, fashion, those that spread widely, and those that terminate in a laterally periodic fashion. In several cases we find evidence for a correlation between specific patterns of projection and known physiological differences between the topographies of laminae that are connected. In cases where two laminae possess similar topographies (for example, where both contain orderly maps for orientation) their interconnections appear precise, with little diffuse spread. In cases where two laminae are characterized by strikingly different topographies (where, for example, one contains an orderly map for orientation and the other a precise map for retinotopic position, but no specificity for orientation), the connections appear more diffuse.

We made focal iontophoretic as well as larger pressure injections (n = 30; 19 used for most analyses) of the tracer biocytin in visual area V4 of six macaque monkeys. The resulting transported label enabled mapping of intrinsic inter- and intralaminar connections within the region. We found that pyramidal neurons of layers 2 and 3 make extensive lateral projections within area V4, with oval or circular patches of terminals in layers 1-3. Any small patch of tissue (approximately 250 microns wide) injected in the superficial layers appeared to connect reciprocally to patches scattered up to 3 mm around the injection. The patches of terminal label measure 250-450 microns across, spaced roughly 600 microns (range, 450-1300 microns) center to center, and where most densely packed they occupy 33% of the cortical area with approximately 3-4 patches/mm2. Small injections in layers 4 and 6 did not produce contributions to these patchlike lattice connections, while injections in layer 5 gave very weak rising contributions to the superficial layer patch system. Large pressure injections of biocytin gave wider spread and more densely labeled patches, but their size and spacing appeared much the same as with small injections. The V4 pattern of label was compared to the patterns seen in areas V1 and V2 after similar-sized injections of biocytin; patches in V1 and V2 were slightly smaller (roughly 250-300 microns across) and more closely spaced (425-450 microns center to center), consistent with earlier measures in these areas using HRP. The peak areal occupancy of patches was approximately the same, 27-33% in each region. We interpret these findings as indicating a functional repeat distance of 450-600 microns in area V4 (fixed tissue measures) with a patchy, discontinuous layout. Given the dimensions of the V4 intrinsic connectional system demonstrated here, it seems unlikely that it relates directly to the topography of specific afferent terminations or efferent neuron groups, which appear from other studies to have a larger scale of repeat (2-3 mm). However, patches in V4 tend to aggregate, forming clusters extended in the mediolateral direction, suggesting a possible relation to coarser connection zones.

The intrinsic connectivity of striate cortex was investigated by injecting horseradish peroxidase (HRP) into this area in tree shrews. Such HRP injections demonstrated periodically organized, stripelike connections within area 17. These stripes occur in layers I-IIIA and consist of a small number or retrogradely filled neurons, some clearly pyramidal, together with HRP-labeled axon terminals. HRP-filled axons trunks run between labeled stripes, interconnecting adjacent and distant regions of the stripe pattern. Correlation with Golgi-stained tissue suggests that these stripes are horizontally interconnected by pyramidal neurons with long intracortical axon collaterals (followed for distances over 1 mm from the soma). The HRP-labeled strips measure about 230 micrometers in width, with a center-to-center repeat distance of 450--500 micrometers. They have been mapped over an 8 mm2 area of striate cortex and would thus seem capable of effecting lateral interactions over considerable portions of the retinotopic map. In their dimensions and overall pattern, these anatomical stripes resemble the 2-deoxyglucose (2-DG) bands resulting from visual stimulation of trees shrews with stripes of a single orientation. While the functional role of the HRP-labeled stripes is unclear, their similarities with the 2-DG pattern raise the intriguing possibility that they may be related to orientation selectivity. The striking regularity of these extensive lateral interconnections emphasizes the importance of horizontal intralaminar connections within the cortex.

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Optical imaging is the video recording of two-dimensional patterns of changes in light reflectance from cortical tissue evoked by stimulation. We derived a method, extended spatial decorrelation (ESD), that uses second-order statistics in space for separating the intrinsic signals into the stimulus related components and the nonspecific variations. The performance of ESD on model data is compared to independent component analysis algorithms using statistics of fourth and higher order. Robustness against sensor noise is scored. When applied to optical images, ESD separates the stimulus specific signal well from biological noise and artifacts.