Quantitative morphology and postsynaptic targets of thalamocortical axons in critical period and adult ferret visual cortex

Thalamocortical axons segregate into ocular dominance columns several weeks before the onset of critical period plasticity in ferret visual cortex, a stage characterized by anatomical changes in thalamic input as a consequence of abnormal visual stimulation. In search of possible anatomical correlates of this plasticity, we examined, at electron microscope resolution, the morphology and the synapsing and target selection properties of thalamic axons in ferret visual cortex during and after the critical period. Adult thalamocortical terminals visualized by anterograde tract-tracing display significantly larger cross-section areas than terminals at postnatal day (P) 35, P40, and P49 critical period ages. They are also significantly larger than nonthalamocortical terminals, which attain an adult-like size distribution by P40. The synaptic zones of adult thalamocortical terminals are significantly larger than those of critical period terminals. Perforated and invaginated synapses are encountered frequently on thalamic axons in both adulthood and the P40-49 age group. This result contradicts the view that synaptic perforations and spinules are indicative of a capacity for plasticity. It also suggests that at least some morphological features of thalamic terminals attain maturity on a developmental schedule that is independent of critical period plasticity. Connectivity properties of labeled axons, however, suggest an active role for thalamocortical axons in the critical period. In P40, P49, and adult brains, 23%, 17%, and 9%, respectively, of all thalamocortical synapses contact GABAergic interneurons, suggesting that thalamic input is more strongly involved in driving inhibitory circuits in young ages. Furthermore, thalamocortical axons in P35-49 brains form about 60% more synapses per axon length than in adult brains, suggesting that stabilization of thalamic synapses at the end of the critical period may be accompanied by a reduction of synaptic contacts, as well as a reorganization of postsynaptic circuit selectivity. (c) 2005 Wiley-Liss, Inc.