The Role of Activity in the Development of Long-Range Horizontal Connections in Area 17 of the Ferret

Abstract

Horizontal connections in area 17 of adult cats and ferrets link cells with similar preferred orientations by a patchy network of projections extending several millimeters across the cortex. The maturation of orientation selectivity in ferret area 17 has been demonstrated previously by quantitative single-unit recording and optical imaging to begin at approximately postnatal days (P) 32-P36. We therefore made restricted injections of cholera toxin B-subunit (CTB) or CTB-gold into ferret area 17 at a series of developmental ages and statistically quantified the degree of clustering in plots of retrogradely labeled cells in tangential sections through layer III for comparison to the published values for orientation tuning at each age. At P21, horizontal connections within area 17 lacked patchiness entirely, although clear patches of labeled cells were present in extrastriate areas. By P27, significant clustering of horizontal connections within area 17 was present. A second phase of cluster refinement was observed to occur at approximately P34-P36, coinciding with the emergence of mature orientation tuning and maps. Continuous silencing of cortical action potentials by chronic tetrodotoxin infusion from P21 resulted in a spatially random distribution of retrogradely labeled cells at P34. In contrast, bilateral enucleation from P21 did not prevent the initial development of clustered horizontal connections. We conclude, based on our findings and those of others, that the anatomical specificity of long-range horizontal connections results from an activity-dependent process that initially can use spontaneous activity in the cortical and thalamic networks to establish crude periodic connections and later uses visual cues to refine these connections.

Rapid plasticity of binocular connections in developing monkey visual cortex (V1)

“…The crude long-range connections, intrinsic or feedback, are largely present in primates at birth (41)(42)(43) by eye opening in kittens (44,45) and by 4 weeks of age in ferrets (46). In cats and ferrets, the refinement of these connections continues to depend on normal visual experience (46,47).…”

Modulation of Intrinsic Circuits by Serotonin 5-HT3Receptors in Developing Ferret Visual Cortex

“…Optical recording provides a faithf ul measure of the spatiotemporal properties of neuronal activity on a circuit level (Grinvald et al, 1982(Grinvald et al, , 1994Albowitz and Kuhnt, 1993;Sutor et al, 1994;Nelson and Katz, 1995;Jackson and Scharfman, 1996;Tanif uji et al, 1996). The depression of circuit activation revealed by optical recording peaked between P32-P35 and P40 -P45, which corresponds to the period of axonal cluster refinement and maturation of orientation tuning in the supragranular layers (Chapman and Stryker, 1993;Dalva and Katz, 1994;Nelson and Katz, 1995;Durack and Katz, 1996;Ruthazer and Stryker, 1996). The main mechanism underlying the circuit inhibition is likely to be activation of the GABAergic network, because on a single-cell level the predominant effect of receptor selective agonists was to increase the frequency of spontaneous GABAergic synaptic currents.…”

“…In the visual system this activity may originate in the retina (Feller et al, 1996;Weliky and Katz, 1997), the lateral geniculate nucleus, and /or the cortex itself (Ruthazer and Stryker, 1996). Intracortical synaptic activity may also be regulated by inputs from brain regions outside the primary visual pathway.…”

Activity-Dependent Regulation of NMDAR1 Immunoreactivity in the Developing Visual Cortex

“…In these superficial layers, the pattern of lateral axonal connections develops over the same time course as that for the geniculocortical axons (Callaway and Katz, 1990;Ruthazer and Stryker, 1996). However, unlike layer 4, in which major axonal remodeling appears to end with the close of the critical period, evidence suggests that the capacity for axonal remodeling of horizontal connections persists in layers 2/3 into adulthood (Darian-Smith and Gilbert, 1994).…”

“…During the segregation of geniculocortical axons to form ocular dominance columns in development, monocular deprivation causes a functional and anatomical expansion of the open eye's cortical territory (Hubel et al, 1977;Shatz and Stryker, 1978;Stryker and Harris, 1986;Antonini and Stryker, 1993a), whereas eliminating all retinal activity in both eyes prevents column formation (Stryker and Harris, 1986). The formation of highly specific horizontal connections between orientation-specific domains in layers 2/3 also requires visual experience (C allaway and Katz, 1991;Ruthazer and Stryker, 1996).…”