Lamina 4C Research Articles

A neuroanatomically-based model for human color vision

Presently there are two dominant theories for human color vision: Young-Maxwell-Helmholtz's trichromatic theory and Hering's opponent-color theory. It is widely purported that the trichromatic theory holds true for retinal color processing whereas the opponent-color theory works for cortical color processing. My purposes in the present paper are threefold: to demonstrate, based on both empirical and logical grounds, that the opponent-color theory is fundamentally untenable; to extend the trichromatic theory from retinal color processing to the cortical level; and to present a computational model based on neuroanatomical data for human color vision. Empirically, the opponent-color theory is false because it runs against many lines of observational and experimental data. First of all, this theory claims that it is impossible for a human being to perceive red and green colors in the same place at the same time; now there have been several demonstrations (e.g., see [1] and [2]) clearly indicating that this assumption is unwarranted. Second, colors appearing in complementary afterimages and in color contrast conditions are complementary to stimulus colors—rather than opponent colors as the opponent theory supposes. Third, in the so-called flight-of-colors phenomenon, the predominant colors are the complementary colors of three primary colors (red, green, and blue) embraced by the trichromatic theory, not the four unique hues (red, green, yellow, and blue) as assumed by the opponent-color theory. Logically, the opponent-color theory needs to postulate a neural mechanism for mixing colors between red and green colors which in turn needs to turn off neural activities along the red and the green cardinalities—it is simply impossible to realize such a mechanism in any physical system. In contrast to the opponent-color theory, the trichromatic color theory can easily be extended to cortical color processing. In fact, such a theoretical integration had been attempted by Rollett [3] and McDougall [4] more than a century ago—It is very unfortunate that their efforts had largely been forgotten. Here I attempt to use an extended Young-Maxwell-Helmholtz trichromatic theory to explain several color perception phenomena, including co-existence of red and green colors, both positive and negative afterimages, contrast colors, and flight-of-colors. Based on the fact that many color phenomena are monocular, I further propose that, in the primate (including the humankind) visual system, lamina 4C in the primary visual cortex (V1) is the neural substrate for cortical trichromaticity—because this is the only cortical stage where neurons are predominantly monocular. I present a three-layer computational model to simulate the first three stages of human visual processing: the retina, the LGN, and layer 4C. By incorporating anatomical data of cell distributions and a scheme of neuronal population cardinality coding, the model can account for many essential features of trichromaticity: additive and subtractive color mixing, color complementarity in afterimages and in contrast colors, and color transparency. Conclusions In summary, I contend that the trichromatic theory can explain both retinal and cortical color processing and that the opponent-color theory is fundamentally erroneous. Furthermore, I suggest that the neuronal trichromatic stage directly corresponding to human color sensation is layer 4C in V1.

Neuropathology provides clues to the pathophysiology of Gaucher disease

To better understand the pathogenesis of brain dysfunction in Gaucher disease (GD), we studied brain pathology in seven subjects with type 1 GD (four also exhibited parkinsonism and dementia), three with type 2 GD and four with type 3 GD. Unique pathologic patterns of disease involving the hippocampal CA2-4 regions and layer 4b of the calcarine cortex were identified. While these findings were common to all three GD phenotypes, the extent of the changes varied depending on the severity of disease. Cerebral cortical layers 3 and 5, hippocampal CA2-4, and layer 4b were involved in all GD patients. Neuronal loss predominated in both type 2 and type 3 patients with progressive myoclonic encephalopathy, whereas patients classified as type 1 GD had only astrogliosis. Adjacent regions and lamina, including hippocampal CA1 and calcarine lamina 4a and 4c were spared of pathology, highlighting the specificity of the vulnerability of selective neurons. Elevated glucocerebrosidase expression by immunohistochemistry was found in CA2-4. Hippocampal 45Ca 2+ uptake autoradiography in rat brain was performed demonstrating that hippocampal CA2-4 neurons, rather than CA1 neurons, were calcium-induced calcium release sensitive (CICR-sensitive). These findings match recent biochemical studies linking elevated glucosylceramide levels to sensitization of CA2-4 RyaR receptors and 300% potentiation of neuronal CICR sensitivity. In two patients with type 1 GD and parkinsonism, numerous synuclein positive inclusions, similar to brainstem-type Lewy bodies found in Parkinson disease, were also found hippocampal CA2-4 neurons. These findings argue for a common cytotoxic mechanism linking aberrant glucocerebrosidase activity, neuronal cytotoxicity, and cytotoxic Lewy body formation in GD.

Intermodal Selective Attention in Monkeys. II: Physiological Mechanisms of Modulation

Of all areas studied in the accompanying study, attention effects were most consistent and well resolved in V4. In this study, to define some of the anatomical circuits and neural processes underlying the influence of attention, we examined the laminar distribution and physiology of attention effects in V4 and in two lower areas, V1 and V2. Laminar event-related potential (ERP), current source density (CSD) and multiunit activity (MUA) profiles allowed identification of processes occurring in the local ensembles, as well as their sequence and laminar distribution. These methods also permitted us to analyze the brain processes reflected in attention-sensitive components of the surface ERP. As outlined in the previous study, the first robust modulation by attention occurred in V4 during the 100-300 ms poststimulus interval. This is the time frame of the net refractoriness which follows the net local excitatory response to luminance increment. Over this interval, attention reduced CSD amplitudes and increased action potential firing rates, findings consistent with disinhibition as a mechanism for attention in V4. Similar effects were observed during the 100-300 ms time frame in V2. In V4, attention had no effect on the initial excitatory response at the depth of lamina 4, but it did produce large modulations in supragranular and deep laminae, origins of both feedforward and feedback projections. Attentional modulation in V2 was later than in V4 and concentrated in extragranular laminae, with no modulation of the initial layer 4 response. Attentional modulation in V1 was smaller and still later than that in V2 and was focused in the supragranular laminae. In this paradigm, attention did not modulate either the response in lateral geniculate nucleus (LGN) or the initial excitation in lamina 4C of V1. The timing of effects across areas and the laminar distribution of effects within areas indicate that attention effects are mediated by feedback projections. Moreover, our findings suggest that attention may increase the perceptual salience of stimuli by reducing stimulus-evoked refractoriness and/or inhibition in cortical ensembles. Finally, attentional modulation of transmembrane current flow in V4 produced a sustained negative deflection in the laminar ERP profile, that was manifested in the ERP over the occipital surface. This posits a mechanism for the 'selection negativity', a scalp ERP effect noted under similar experimental conditions in human subjects.

Columnar activity regulates astrocytic beta-adrenergic receptor-like immunoreactivity in V1 of adult monkeys.

Recent results indicate that astrocytic beta-adrenergic receptors (beta AR) participate in noradrenergic modulation of synaptic activity. In this study, we sought to examine whether neural activity can, in turn, regulate astrocytic beta AR. To address this question, an antiserum that recognizes beta-adrenergic receptors (beta AR) specifically in astrocytes was used to assess the distribution of the receptors across ocular dominance columns in V1 of two monocular and four visually intact adult monkeys. Cytochrome oxidase histochemistry (CO) was used to identify the position of the cortical laminae and of the ocular dominance columns receiving visual inputs from the intact and enucleated eyes. This stain revealed the expected pattern within V1 of monocular monkeys--i.e. darker and lighter bands of equal widths (ca. 500 microns) spanning laminae 4-6, each associated with larger and smaller blobs, respectively, in lamina 2/3. Alignment of CO sections with adjacent sections stained for astrocytic beta AR by the immunoperoxidase method revealed intense beta AR-like immunoreactivity (beta AR-li) in the superficial laminae, a slightly weaker staining in the infragranular laminae and weakest staining in lamina 4C. Within lamina 4C, a prominent striped pattern was evident. The darker bands of the stripe closely matched widths and positions of the lighter CO columns associated with the enucleated eye. On the other hand, immunocytochemical staining for the astrocytic intermediate filament protein, GFAP, within V1 of monocular monkeys revealed no inter-columnar difference in the density of astrocytic cell bodies or processes. Nissl stain also revealed no overt inter-columnar differences in cell density.(ABSTRACT TRUNCATED AT 250 WORDS)

Nitric oxide synthase in the visual cortex of monocular monkeys as revealed by light and electron microscopic immunocytochemistry

Recent results indicate that nitric oxide (NO) can play an important role in excitability by modifying the strength of activated synpases and regulating local cerebral blood flow. We sought to determine whether the level of NO synthase (NOS) could, in turn, also be regulated by neural activity. Results using a polyclonal anti-NOS antibody showed that, in cortical area V1 of monocular monkeys. NOS-immunoreactivity is diminished in lamina 4C neuropil of the deprived ocular dominance columns relative to the immediately adjacent non-deprived columns. Closer examination of lamina 4C indicated that the intercolumnar difference in NOS-immunoreactivity does not reflect differences in the distribution of NOS-labeled perikarya, since relatively few neurons were immunoreactive for NOS in lamina 4C of either monocular or normal binocular monkeys. Electron microscopy revealed that the majority (> 80%) of NOS-immunoreactive profiles in lamina 4C are axon terminals. NOS-immunoreactive spines and dendritic shafts also are present but these are more prevalent in the superficial laminae. In order to determine whether the intercolumnar differences in lamina 4C neuropil correspond to altered densities of NOS cells in the superficial laminae, we performed a series of quantitative analyses. In the superficial laminae, NOS-cells occur as two distinguishable classes: a few that are large and intensely NOS-immunoreactive and many more (ca. 24-fold) that are small and lightly immunoreactive. Analysis of the distribution of 559 small and 105 large NOS-immunoreactive cells within 40-μm-thick tangential sections spanning laminae 2–3 showed that the number of cells (large and small together) associated with each blob is approximately 14 for both deprived (lighter) and non-deprived (darker) blobs. These cells are distributed evenly from the center to periphery of columns. Analysis of the distribution of NOS-cells in the infragranular laminae also did not reveal any columnar differences. These observations suggest that local neural activity may be coupled to NO release via alteration of NOS protein levels specifically within distal axonal processes of neurons. Thi s mechanism could operate in conjunction with the more instantaneous catalytic activation of NOS. Ultrastructural analyses further suggest that NO may act as an anterograde and retrograde messenger arising from terminals in addition to its proposed role as a retrograde messenger arising from dendrites.

Interpretation of high-resolution current source density profiles: a simulation of sublaminar contributions to the visual evoked potential.

Current source density (CSD) analysis provides an index of the location, direction, and density of transmembrane currents that arise with synchronous activation of neural tissue and that generate an evoked potential profile in the extracellular medium. In neocortex and other laminated structures, a simplified, one-dimensional CSD analysis can be computed by differentiation of voltages sampled at discrete points in a linear array. One-dimensional CSD analysis is a practical and accurate method for defining both regional activity patterns and neural generators of surface-recorded evoked and event-related potentials. In computing the CSD, common practices of differentiating across spatial grids of 200 microns or more and use of spatial smoothing routines help to reduce noise, but severely limit the spatial resolution available to the analysis. High-resolution CSD procedures (i.e., 3 point differentiation using a spatial grid of 100 microns or less) are more suited to identification of processes within individual cortical laminae or sublaminae, but can magnify the contributions of computational artifacts. Despite the inclusion of independent indices of cellular activity (e.g., multiunit activity), both high- and low-resolution analyses may indicate current source and sink configurations for which there is more than one plausible physiological interpretation. In the present study we examined the resolving capacity and pitfalls of common CSD procedures using simulated ensembles of current dipoles. These were positioned and oriented to model the depolarization of lamina 4C stellate cells and thalamocortical afferents in macaque striate cortex. Empirically, the surface N40 appears in association with a CSD configuration which includes current sinks within the thalamorecipient (stellate) subdivisions of lamina 4C and a large current source extending considerably below 4C. Dipole ensemble contributions to the CSD profile were computed and compared to physiological data from this region. Small asymmetries in activation of model stellate laminae were sufficient to produce substantial open field contributions. However, the best fit with empirical CSD profile was found when the simulation included contributions from thalamocortical axons, along with both open and closed field contributions from dual stellate cell sublaminae. High-resolution CSD profiles were shown to be interpretable when computational artifacts characteristic of closed and open fields were identified using a series of differentiation grids.

Postnatal development of thalamic recipient neurons in the monkey striate cortex: Comparison of spine acquisition and dendritic growth of layer 4C alpha and beta spiny stellate neurons

A quantitative study has been made from Golgi impregnations of the maturation of dendrites and their spines on spiny stellate neurons in the macaque monkey primary visual cortex. The neurons studied lay within either the alpha or the beta division of lamina 4C; previous workers have shown the alpha division neurons to be contacted by thalamic axon terminals arising from the magnocellular division of the lateral geniculate nucleus (LGN) of the thalamus and the beta division neurons to be contacted by parvocellular LGN inputs. Most thalamic terminals and perhaps the majority of other type 1 (Colonnier, '81), presumed excitatory, inputs to these cells make synaptic contacts on the tips of their dendritic spines. Measurement was made of relative changes in the total number of spines on these alpha and beta spiny neurons over age by measuring both spine density along the dendrites and dendritic arbor size in single 90-microns sections from Golgi rapid preparations. Our previous work (Lund et al., '77; Boothe et al., '79) showed a marked proliferation and attrition of spines and dendritic branches to occur in the early postnatal weeks; Rakic et al. ('86) have since proposed that there is a cortexwide synchrony of synapse acquisition and loss during this same period. However, different visual capacities channelled via the magnocellular and parvicellular geniculate relays show different maturational rates (Harwerth et al., '86). This study indicates that the anatomical maturation of spines on the alpha and beta neurons is not temporally coincident from birth to 30 weeks. During this period, phases of spine acquisition and loss on alpha neurons precedes similar phases on beta neurons. The alpha neurons carry a peak spine population at 5-8 weeks postnatal, whereas the beta neurons carry their peak spine populations between 8 and 24 weeks postnatal. At all ages prior to 30 weeks, the two sets of neurons carry quite different total spine populations. Close to 30 weeks of age, the total spine coverage has fallen on both sets of neurons and becomes identical between the alpha and beta neurons. In animals aged 30 weeks to adult, spine coverage per neuron is maintained at a common figure for the alpha and beta neurons despite further growth and disparate dendritic arbor sizes and different local spine densities in the two groups; this suggests that some common sampling paradigm between pre- and postsynaptic elements is adopted by the alpha and beta neurons and also suggests the development of a close functional correlation between the two sets of neurons.

Striate cortical contribution to the surface-recorded pattern-reversal vep in the alert monkey

The striate cortical contribution to the surface pattern-reversal visual evoked potential (VEP) was investigated in awake monkeys during performance of a visual fixation task, by examining laminar profiles of VEP, current source density (CSD) and concomitant multiunit activity (MUA) in Area 17, recorded simultaneously at incremental depths using multicontact electrodes. Stimuli were black/white bar gratings centered on the fixation point. The typical surface pattern-reversal VEP over striate cortex consists of a prominent positivity peaking at 50–70 msec (P60), followed by a large negativity peaking at approx. 80 msec (N80), and then by a late broad positivity, peaking between 120 and 150 msec (P125). P60 is often preceded by a small negativity peaking at 45–55 msec (N50), and on rare occasions a small positivity (P40) is also observed. N50 is generated primarily by current sinks in Lamina 4C. P60 arises from large current sources in the supragranular laminae. N80 and P125 appear to be composite waveforms reflecting complex contributions from local activity and from activity occurring outside of the foveal/immediate parafoveal representation in Area 17. The basic physiologic sequence elicited by patterned stimulation is similar to that elicited by diffuse luminance or by electrical stimulation, but is characterized by more prominent supra- and infragranular activation. It is consistent with the cellular and synaptic anatomy of Area 17: initial activation of the thalamorecipient subdivisions of Lamina 4C, followed by activation of mid/upper Lamina 4 and of supra- and infragranular laminae. Our results suggest the possibility of differentiating synaptic stages and cellular processes reflected in the human VEP, based on homologies with simian VEP components.

Distribution of GABAergic neurons and axon terminals in the macaque striate cortex.

Antisera to glutamic acid decarboxylase (GAD) and gamma-aminobutyric acid (GABA) have been used to characterize the morphology and distribution of presumed GABAergic neurons and axon terminals within the macaque striate cortex. Despite some differences in the relative sensitivity of these antisera for detecting cell bodies and terminals, the overall patterns of labeling appear quite similar. GABAergic axon terminals are particularly prominent in zones known to receive the bulk of the projections from the lateral geniculate nucleus; laminae 4C, 4A, and the cytochrome-rich patches of lamina 3. In lamina 4A, GABAergic terminals are distributed in a honeycomb pattern which appears to match closely the spatial pattern of geniculate terminations in this region. Quantitative analysis of axon terminals that contain flat vesicles and form symmetric synaptic contacts (FS terminals) in lamina 4C beta and in lamina 5 suggest that the prominence of GAD and GABA axon terminal labeling in the geniculate recipient zones is due, at least in part, to the presence of larger GABAergic axon terminals in these regions. GABAergic cell bodies and their initial dendritic segments display morphological features characteristic of nonpyramidal neurons and are found in all layers of striate cortex. The density of GAD and GABA immunoreactive neurons is greatest in laminae 2-3A, 4A, and 4C beta. The distribution of GABAergic neurons within lamina 3 does not appear to be correlated with the patchy distribution of cytochrome oxidase in this region; i.e., there is no significant difference in the density of GAD and GABA immunoreactive neurons in cytochrome-rich and cytochrome-poor regions of lamina 3. Counts of labeled and unlabeled neurons indicate that GABA immunoreactive neurons make up at least 15% of the neurons in striate cortex. Layer 1 is distinct from the other cortical layers by virtue of its high percentage (77-81%) of GABAergic neurons. Among the other layers, the proportion of GABAergic neurons varies from roughly 20% in laminae 2-3A to 12% in laminae 5 and 6. Finally, there are conspicuous laminar differences in the size and dendritic arrangement of GAD and GABA immunoreactive neurons. Lamina 4C alpha and lamina 6 are distinguished from the other layers by the presence of populations of large GABAergic neurons, some of which have horizontally spreading dendritic processes. GABAergic neurons within the superficial layers are significantly smaller and the majority appear to have vertically oriented dendritic processes.(ABSTRACT TRUNCATED AT 400 WORDS)

Local circuit neurons of macaque monkey striate cortex: I. Neurons of laminae 4C and 5A.

A study has been made, using Golgi preparations, of the organization of neurons with smooth or sparsely spined dendrites, here called local circuit neurons, of the macaque monkey primary visual cortex. Since these neurons include those responsible for inhibitory circuitry of the cortex, a better understanding of their anatomical organization is essential to concepts of functional organization of the region. This account describes those neurons found with cell body and major dendritic spread within the thalamic recipient zone of lamina 4C and its border zone with lamina 5A. The neurons are grouped firstly in terms of in which laminar division the soma occurred--4C beta, 4C alpha or the border zone of 5A-4C beta--and secondly, into varieties on the basis of the interlaminar projection patterns of their axons. Most, if not all, of the local circuit neurons of these divisions have interlaminar axon projections as well as an arbor local to their cell body and dendritic field. These interlaminar projections are highly specific, targeting from one to five laminar divisions depending on the variety of neuron; on this basis 17 varieties of local circuit neuron are described. While the number of varieties appears dauntingly large in terms of understanding the functional circuitry of the region, the clear-cut organization of the interlaminar links may provide clues as to the information processing that concerns each neuron. The local circuit neuron axon projections can be related to a wealth of information already available concerning the laminar organization of afferent axons and efferent cell groups, the organization of spiny neuron intrinsic relays (presumed to be excitatory), and physiological properties of different laminar divisions. It is hoped that the information derived from this study can serve as a guide for correlated physiological-anatomical studies on single cells of the region.

Intrinsic connections of macaque striate cortex: afferent and efferent connections of lamina 4C

We have studied the intrinsic organization of macaque striate cortex by tracing the pattern of horseradish peroxidase (HRP)-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 4C alpha and 4C beta differ in their pattern of projections to the superficial layers of striate cortex. Axons from neurons in lamina 4C beta ascend through lamina 4B without giving off collaterals and terminate in lamina 4A and in the base of lamina 3. By contrast, axons from neurons in lamina 4C alpha terminate in lamina 4B and less densely in the 4A/3B region. The projection from lamina 4C beta to lamina 4A is particularly dense and is distributed in a patchy fashion immediately above each injection site. The projection from lamina 4C beta to lamina 3B appears less dense and more widespread; we estimate that individual 4C beta axons may spread laterally for more than 400 micron. Furthermore, the pattern of HRP-labeled cell bodies in lamina 4C beta following injections into laminae 4A and 3B provides evidence for a subdivision within 4C beta. These injections always produce a large number of labeled neurons in the upper part of lamina 4C beta, whereas the lower portion contains few labeled neurons that are located immediately under the center of the injection site. Both lamina 4C alpha and lamina 4C beta also contribute less dense projections to the deeper layers of cortex. Lamina 4C beta projects mainly to lamina 6, whereas lamina 4C alpha contributes axon terminals to both lamina 5A and lamina 6. Neurons in lamina 6 provide the bulk of the intracortical projections to lamina 4C. The axons of these neurons are fine in caliber and have a delicate side-spine morphology that is quite distinct from lateral geniculate axon arbors. Neurons in lamina 5A also project onto lamina 4C, but the projections of these neurons appear concentrated in lamina 4C alpha. 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.

Intrinsic connections of macaque striate cortex: axonal projections of cells outside lamina 4C

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.

Physiological organization of layer 4 in macaque striate cortex

Numerous highly angled electrode penetrations through the opercular region of macaque striate cortex reveal that layers 4A, 4C alpha, and 4C beta--the primary input sublaminae for axons from the lateral geniculate nucleus (LGN)--are retinotopically organized on a fine scale and populated mostly by monocularly driven cells having small receptive fields and lacking orientation selectivity. Layer 4B, which does not receive a direct thalamic input, contains orientationally selective cells, and many of these are also direction selective. To a significant degree the response properties of cells in layers 4C alpha and 4C beta reflect the response properties of their respective afferent inputs, from the magno- and parvocellular laminae of the LGN. Accordingly, cells in layer 4C alpha have lower contrast thresholds and larger minimum response fields than do the cells in layer 4C beta. In contrast to this clear-cut separation, the cells of layer 4A (whose major source of direct LGN input arises from the parvocellular layers) exhibit both high and low contrast thresholds. With regard to the precision of retinotopic mapping that is seen in lamina 4C, it is noteworthy that there is substantial overlap among the minimum response fields of neighboring neurons. Due to a larger mean receptive field size, this overlap is greater in layer 4C alpha than it is in 4C beta. In either sublamina, however, the minimum cortical distance that separates different and nonoverlapping parts of the visual field corresponds closely--within a factor of 2--to the known arborizational spreads of single geniculate afferents.

Neuronal composition and development in lamina 4C of monkey striate cortex.

Lamina 4C (Lund, '73) of the monkey, Macaca nemestrina, visual striate cortex occupies a key position as a principal recipient zone of axons from the lateral geniculate nucleus (LGN). Synaptic maturation in lamina 4C is of particular interest since it involves a competitive interaction between thalamic axons for postsynaptic territory: an interaction which is strongly influenced by afferent activity (Hubel et al., '77). As an initial step toward understanding the normal process of synapse maturation in 4C, this study examines Golgi material to define the adult neuron populations of subdivisions 4C alpha (receiving afferents from magnocellular LGN) and 4C beta (receiving afferents from parvocellular LGN). Three groups of spine-bearing neurons are described--one relatively confined to either alpha or beta subdivision, the other two bridging the depth of 4C; four groups of smooth dendritic neurons interact with the spine-bearing population. Electron microscopy of normal and Golgi-impregnated tissue is used to define key features of synapse populations on these neurons. From embryonic day 159 through adulthood the smooth and spiny neurons occur in the same constant proportions in the neuropil (5% smooth, 95% spiny). Changes in the distribution of synapses on the spiny neurons are analyzed qualitatively; type 1 axon terminals (asymmetric apposition--round vesicles) shift from dendritic shafts to spine tips during maturation. Each spine is found to bear a type 1 contact at all ages; these results allow us to conclude that the figures of Boothe et al. ('79) on changes in spine populations during maturation can now be interpreted as changes in type 1 synapse populations. It is shown that type 2 synapses (symmetric appositions--pleomorphic vesicles) arise from axons of the smooth dendritic neurons. These synapses are found to increase in number on the spiny cell somata in early postnatal development, and this is followed by a decrease in number to the adult level.

Spine formation and maturation of type 1 synapses on spiny stellate neurons in primate visual cortex

This study continues an investigation (Mates and Lund, '83a) of neuronal development in lamina 4C of macaque monkey striate visual cortex. The maturational history of the type 1 synaptic contacts on spine-bearing stellate neurons, which comprise 95% of the neurons of the lamina, is described. It is shown that type 1 contacts are initially found on the dendritic shafts; these contacts appear to be carried out on spine outgrowths. This leads to the adult condition where type 1 contacts are found only on the spine tips. A similar phenomenon has been reported for pyramidal neurons of the rat (reported during the course of this study by Miller and Peters, '81). In later maturation the spine and its type 1 contact may be lost; profiles found in the neuropil illustrate a process of shrinkage and detachment of both the type 1 axon terminals and postsynaptic dendritic spines in normal maturation. These findings provide an explanation for the marked increase and decrease in spine populations observed to occur on these neurons during normal maturation in an earlier study by Boothe et al. ('79).

Developmental changes in the relationship between type 2 synapses and spiny neurons in the monkey visual cortex.

This study continues an exploration of synaptic development in the primary visual cortex of the monkey (Macaca nemestrina). In a prior study (Mates and Lund, '83a), we observed that type 2 synapses on the cell bodies of spiny stellate neurons of lamina 4C appeared not only to increase in number during early postnatal development but also subsequently decreased during maturation. Using quantitative, stereological electron microscopic methods, we examined the maturation of this synapse population from embryonic day 159 to adult, on spiny stellate neurons of 4C alpha and beta and, for comparison, on pyramidal neurons in upper and lower lamina 6. Tissue was also taken for comparison from two animals reared to 8 weeks of age with binocular eyelid closure from birth. We confirmed that a marked increase and subsequent decrease occurred in this somal type 2 synapse population on both neuron populations. However, due to the infrequency of the smooth dendritic neurons (approximately 5% of the neuron population) giving rise to the type 2 contacts, and due to expansion of the neuropil during maturation increasing intercell distances against constant volume of the type 2 axon arbors, it is concluded that the decrease in type 2 somal synapses may represent a redistribution to dendrites rather than loss from the neuropil. Cells of lamina 4C beta (receiving input from the parvocellular lateral geniculate nucleus-LGN) show a slower initial accumulation of type 2 contacts compared to neurons of lamina 4C alpha (receiving input from magnocellular LGN), or to pyramidal neurons of lamina 6.(ABSTRACT TRUNCATED AT 250 WORDS)

Ordinal position and afferent input of neurons in monkey striate cortex.

From the extracellular recording of single units in the monkey striate cortex and electrical stimulation at two selected sites in the optic radiations it was possible to estimate 1) the ordinal position of striate neurons (i.e., whether they received a monosynaptic, disynaptic or polysynaptic input from the thalamus) and 2) the nature of the afferent input to these neurons (i.e., whether it came from the magnocellular or parvocellular subdivision of the lateral geniculate nucleus (LGN)). Based on receptive field properties six major classes of striate neuron were identified--three which lacked orientation specificity (the ON-center, the OFF-center, and the ON/OFF or nonoriented (N-0) receptive fields) and three with orientation specific responses (the S, the C, and the B categories of receptive field). Units lacking orientation specificity were concentrated in laminae 4A, 4C beta and 6 while, for the cells with orientation specificity, C cells were found in laminae 4B and 6, B cells in 2/3 and 5, and S cells predominantly in laminae 2/3, 4C alpha, and 5. The results of electrical stimulation indicated that cell-to-cell transmission time in the monkey striate cortex is 1.5 msec, and latency measures showed that cells with a monosynaptic drive from the thalamus were confined to laminae 4 and 6 while disynaptically driven cells were found principally in upper lamina 4 (4A and 4B). No cell class was identified exclusively with a given ordinal position and there were many types of potential first-order neurons. The conduction time from one stimulating electrode to the next in the optic radiation was used to identify the afferent input to each striate neuron. The input to color-coded neurones was found to come exclusively from parvocellular layers while the C cells and two subclasses of the S cell (S2 and S3) were driven predominantly by the magnocellular subdivision. For other cell types (those with ON-center, N-0, and S1 receptive fields) the input came from either type of LGN neuron. The laminar distribution of neurons receiving a direct input from the magnocellular and parvocellular streams is in accord with the results of anatomical studies into the site of termination of the LGN input. The cell types receiving these direct inputs vary in the two streams so that the parvocellular input terminates on cells with ON-center and N-0 receptive fields in lamina 4C beta while the magnocellular input goes to cells with S, ON-center, N-0, and C receptive fields in lamina 4C alpha and the lower part of 4B. Consideration is given to the influence of these results on models for neural processing in monkey striate cortex and a comparison is drawn with the results of similar studies in the cat.