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, 4Cα, and 4Cβ-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 4Cα and 4Cβ reflect the response properties of their respective afferent inputs, from the magno- and parvocellular laminae of the LGN. Accordingly, cells in layer 4Cα have lower contrast thresholds and larger minimum response fields than do the cells in layer 4Cβ 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 4Cα than it is in 4Cβ. 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

Termination of Afferent Axons in Macaque Striate Cortex

We used horseradish peroxidase (HRP) to orthogradely label afferent axons in macaque striate cortex. Of the 38 axons that we recovered, nine were recorded intracellularly 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 4Cβ, which have extremely circumscribed, dense terminal fields (small branches of which occasionally intrude into 4Cα) 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 4Cα, which have few or no collaterals in layer 6; and (5) afferents to the upper half of layer 4Cα, which have arborizing collaterals in layer 6B. Of the nine axons that were recorded intracellularly, those with projections to layer 4Cβ (two axons) and to layer 1 (one axon) had color-selective properties, whereas those (six axons) which arborized in 4Cα 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 4Cα were found to cover approximately 6 times as much surface area as afferents to 4Cβ. 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 4Cα suggest that individual 4Cα axons supply more than one ocular dominance stripe. In one case where the terminal arborization of a 4Cα 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

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, 4Cα, and 4Cβ-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 4Cα and 4Cβ reflect the response properties of their respective afferent inputs, from the magno- and parvocellular laminae of the LGN. Accordingly, cells in layer 4Cα have lower contrast thresholds and larger minimum response fields than do the cells in layer 4Cβ 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 4Cα than it is in 4Cβ. 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

Termination of afferent axons in macaque striate cortex

We used horseradish peroxidase (HRP) to orthogradely label afferent axons in macaque striate cortex. Of the 38 axons that we recovered, nine were recorded intracellularly 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 4Cβ, which have extremely circumscribed, dense terminal fields (small branches of which occasionally intrude into 4Cα) 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 4Cα, which have few or no collaterals in layer 6; and (5) afferents to the upper half of layer 4Cα, which have arborizing collaterals in layer 6B. Of the nine axons that were recorded intracellularly, those with projections to layer 4Cβ (two axons) and to layer 1 (one axon) had color-selective properties, whereas those (six axons) which arborized in 4Cα 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 4Cα were found to cover approximately 6 times as much surface area as afferents to 4Cβ. 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 4Cα suggest that individual 4Cα axons supply more than one ocular dominance stripe. In one case where the terminal arborization of a 4Cα 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

Sound localization by the barn owl (Tyto alba) measured with the search coil technique

The dynamics and accuracy of sound localization by the barn owl (Tyto alba) were studied by exploiting the natural head-orienting response of the owl to novel sound stimuli. Head orientation and movement were measured using an adaptation of the search coil technique which provided continuous high resolution azimuthal and elevational information during the behavior. The owls responded to sound sources with a quick, stereotyped head saccade; the median latency of the response was 100 ms, and its maximum angular velocity was 790°/s. The head saccade terminated at a fixation point which was used to quantify the owl's sound localization accuracy. When the sound target was located frontally, the owl's localization error was less than 2° in azimuth and elevation. This accuracy is superior to that of all terrestrial animals tested to date, including man. When the owls were performing open-loop localization (stimulus off before response begins), their localization errors increased as the angular distance to the target increased. Under closed-loop conditions (stimulus on throughout response), the owls again committed their smallest errors when localizing frontal targets, but their errors increased only out to target angles of 30°. At target angles greater than 30°, the owl's localization errors were independent of target location. The owl possesses a frontal region wherein its auditory system has maximum angular acuity. This region is coincident with the owl's visual axis

Relation between patterns of intrinsic lateral connectivity, ocular dominance, and cytochrome oxidase-reactive regions in macaque monkey striate cortex

To help understand the role of long-range, clustered lateral connections in the superficial layers of macaque striate cortex (area VI), we have examined the relationship of the patterns of intrinsic connections to cytochrome oxidase (CO) blobs, interblobs, and ocular dominance (OD) bands, using biocytin based neuroanatomical tracing, CO histochemistry, and optical imaging. Microinjections of biocytin in layer 3 resulted in an asymmetric field (average anisotropy of 1.8; maximum spread—3.7 mm) of labeled axon terminal clusters in layers 1-3, with the longer axis of the label spread oriented orthogonal to the rows of blobs and imaged OD stripes, parallel to the V1/V2 border. These labeled terminal patches (n = 186) from either blob or interblob injections (a = 20) revealed a 71 % (132 out of 186) commitment of patches to the same compartment as the injection site; 11 % (20 out of 186) to the opposite compartment and 18 % (34 out of 186) to borders of blob— interblob compartments, indicating that the connectivity pattern is no