There is considerable controversy over the existence of orientation and direction sensitivity in lateral geniculate nucleus (LGN) neurons. Claims for the existence of these properties often were based upon data from cells tested well beyond their peak spatial frequencies. The goals of the present study were to examine the degree of orientation and direction sensitivity of LGN cells when tested at their peak spatial and temporal frequencies and to compare the tuning properties of these subcortical neurons with those of visual cortex. For this investigation, we used conventional extracellular recording to study orientation and direction sensitivities of owl monkey LGN cells by stimulating cells with drifting sinusoidal gratings at peak temporal frequencies, peak or higher spatial frequencies, and moderate contrast. A total of 110 LGN cells (32 koniocellular cells, 34 magnocellular cells, and 44 parvocellular cells) with eccentricities ranging from 2.6 deg to 27.5 deg were examined. Using the peak spatial and temporal frequencies for each cell, 41.8% of the LGN cells were found to be sensitive to orientation and 19.1% were direction sensitive. The degree of bias for orientation and direction did not vary with eccentricity or with cell class. Orientation sensitivity did, however, increase, and in some cases orientation preferences changed, at higher spatial frequencies. Increasing spatial frequency had no consistent effect on direction sensitivity. Compared to cortical cell orientation tuning, the prevalence and strength of LGN cell orientation and direction sensitivity are weak. Nevertheless, the high percentage of LGN cells sensitive to orientation even at peak spatial and temporal frequencies reinforces the view that subcortical biases could, in combination with activity-dependent cortical mechanisms and/or cortical inhibitory mechanisms, account for the much narrower orientation and direction tuning seen in visual cortex.

The koniocellular (K) pathway is one of three pathways from the lateral geniculate nucleus (LGN) to primate visual cortex (V1). K pathway projections to the cytochrome oxidase (CO) blobs of V1 suggest involvement in chromatic processing given reports that the CO blobs in diurnal primates contain cells selective for color. K LGN layers and CO blobs, however, are also well developed in nocturnal primates such as owl monkeys, which are likely to be color blind. Thus, the K pathway plays either different roles in different species or some as yet unidentified common role(s). Because synaptic arrangements underlie functional mechanisms, the purpose of this investigation was to compare the synaptic circuitry related to the K pathway within the CO blobs of two diurnal primates (macaque monkeys and squirrel monkeys) and one nocturnal primate (owl monkey). Presynaptic K axons were labeled with wheat germ agglutinin-HRP, and presynaptic and postsynaptic profiles in CO blobs were identified with post-embedding immunocytochemistry for GABA and glutamate. In all three species, K axon terminals are glutamatergic and larger than local axon terminals, suggesting that they have a greater impact on postsynaptic CO blob targets than signals arriving via layer IV from the P or M pathways. A greater proportion of K axons, however, synapse with larger glutamatergic shafts in the diurnal monkeys than in the nocturnal owl monkey, perhaps reflecting the importance of color within the K pathway of these diurnal species. Alternatively, the loss of color vision in the owl monkey could impact K pathway circuitry earlier in the pathway. The basic similarities between K axon circuitry within the CO blobs of the three primate species examined also could indicate that this pathway plays some common role or roles across species.

As in other primates, the lateral geniculate nucleus (LGN) of owl monkeys contains three anatomically and physiologically distinct relay cell classes, the magnocellular (M), parvocellular (P), and koniocellular (K) cells. M and P LGN cells send axons to the upper and lower tiers of layer IV, and K cells send axons to the cytochrome oxidase (CO) blobs of layer III and to layer I of primary visual cortex (V1). Our objective was to compare the synaptic arrangements made by these axon classes. M, P, and K axons were labeled in adult owl monkeys by means of injections of wheat germ agglutinin-horseradish peroxidase into the appropriate LGN layers. The neurochemical content of both pre- and postsynaptic profiles were identified by postembedding immunocytochemistry for gamma-aminobutyric acid (GABA) and glutamate. Our key finding is that the synaptic arrangements made by M, P, and K axons in owl monkey exhibit more similarities than differences. They are exclusively presynaptic, contain glutamate and form asymmetric synapses mainly with glutamate-positive dendritic spines. The majority of the remaining axons synapse with glutamatergic dendritic shafts. There are also differences between LGN pathways. M and P terminals are significantly larger and more likely to make multiple synapses than K axons, although M and P axons do not differ from each other in either of these characteristics. Of interest, a larger percentage of M and K axons than P axons make synapses with GABAergic dendritic shafts. Cells directly postsynaptic to M and K axons are known to exhibit orientation selectivity and, in some cases, direction selectivity. Cells postsynaptic to P axons do not show these properties, but instead tend to reflect their LGN inputs more faithfully; therefore, it is possible that these physiologic differences seen in the cortical cells postsynaptic to different LGN pathways reflect the differential involvement of inhibitory circuits.

No abstract

Glutamate is used as an excitatory neurotransmitter by the koniocellular (K), magnocellular (M), and parvocellular (P) pathways to transfer signals from the primate lateral geniculate nucleus (LGN) to primary visual cortex (V1). Glutamate acts through both fast ionotropic receptors, which appear to carry the main sensory message, and slower, modulatory metabotropic receptors (mGluRs). In this study, we asked whether mGluR5 relates in distinct ways to the K, M, and P LGN axons in V1. To answer this question, we used light microscopic immunocytochemistry and preembedding electron microscopic immunogold labeling to determine the localization of mGluR5 within the layers of V1 in relation to the K, M, and P pathways in macaque and squirrel monkeys. These pathways were labeled separately via wheat germ agglutinin–horseradish peroxidase (WGA–HRP) injections targeting the LGN layers. mGluR5 is of interest because it: 1) has been shown to be expressed in the thalamic input layers; 2) appears to be responsible for some types of oscillatory firing, which could be important in the binding of visual features; and 3) has been associated with a number of sensory-motor gating-related pathologies, including schizophrenia and autism. Our results demonstrated the presence of mGluR5 in the neuropil of all V1 layers. This protein was lowest in IVCα (M input) and the infragranular layers. In layer IVC, mGluR5 also was found postsynaptic to about 30% of labeled axons, but the distribution was uneven, such that postsynaptic mGluR5 label tended to occur opposite smaller (presumed P), and not larger (presumed M) axon terminals. Only in the K pathway in layer IIIB, however, was mGluR5 always found in the axon terminals themselves. The presence of mGluR5 in K axons and not in M and P axons, and the presence of mGluR5 postsynaptic mainly to smaller P and not larger M axons suggest that the response to the release of glutamate is modulated in distinct ways within and between the parallel visual pathways of primates.