Ordinal position and afferent input of neurons in monkey striate cortex

Abstract

From the extracellular recording of single units in the monkey [Macaca nemestrina] striate cortex and electrical stimulation at 2 selected sites in the optic radiations it was possible to estimate the ordinal position of striate neurons (i.e., whether they received a monosynaptic, disynaptic or polysynaptic input from the thalamus) and 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 6 major classes of striate neuron were identified: 3 classes lacked orientation specificity (the ON-center, the OFF-center and the ON/OFF or nonoriented (N-0) receptive fields) and 3 classes showed orientation specific responses (the S, C and B categories of receptive field). Units lacking orientation specificity were concentrated in laminae 4A, 4C.beta. and 6. For the cells with orientation specificity, C cells were found in laminae 4B and 6, B cells occurred in 2/3 and 5, and S cells occurred predominantly in laminae 2/3, 4C.alpha. and 5. Electrical stimulation indicated that cell-to-cell transmission time in the monkey striate cortex was 1.5 ms. Latency measures showed that cells with a monosynaptic drive from the thalamus were confined to laminae 4 and 6; 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 1st-order neurons. The conduction time from 1 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 neurons was exclusively from parvocellular layers. The C cells and 2 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 correlates with the anatomy into the site of termination of the LGN input. The cell types receiving these direct inputs vary in the 2 streams so that the parvocellular input terminates on cells with ON-center and N-0 receptive fields in lamina 4C.beta.. 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. Models for neural processing in monkey striate cortex are considered and a comparison with the cat is drawn.