Sensory Experience Restructures Thalamocortical Axons during Adulthood

Abstract

SUMMARY The brain’s capacity to rewire is thought to diminish with age. It is widely believed that development stabilizes the synapses from thalamus to cortex and that adult experience alters only synaptic connections between cortical neurons. Here we show that thalamocortical (TC) inputs themselves undergo massive plasticity in adults. We combined whole-cell recording from individual thalamocortical neurons in adult rats with a recently developed automatic tracing technique to reconstruct individual axonal trees. Whisker trimming substantially reduced thalamocortical axon length in barrel cortex but not the density of TC synapses along a fiber. Thus, sensory experience alters the total number of TC synapses. After trimming, sensory stimulation evoked more tightly time-locked responses among thalamorecipient layer 4 cortical neurons. These findings indicate that thalamocortical input itself remains plastic in adulthood, raising the possibility that the axons of other subcortical structures might also remain in flux throughout life.

Cortical fosGFP Expression Reveals Broad Receptive Field Excitatory Neurons Targeted by POm

“…Neurons within the interpolaris division of the spinal trigeminal complex (Sp5i) typically respond to multiple whiskers and project to POm, but they also show a sparse projection to VPM (Veinante et al, 2000). While VPM neurons can respond to multiple whiskers (Nicolelis et al, 1993;Simons and Carvell, 1989), they are dominated by a single-whisker input (Brecht and Sakmann, 2002;Friedberg et al, 1999;Waite, 1973) and project to single cortical barrel columns (Oberlaender et al, 2012;Pierret et al, 2000). POm neurons respond equally well to the stimulation of multiple individual whiskers (Diamond et al, 1992;Masri et al, 2008;Sosnik et al, 2001), and their cortical axonal projections spread across multiple cortical columns (Ohno et al, 2012;Wimmer et al, 2010).…”

Deep Cortical Layers Are Activated Directly by Thalamus

“…S1D, E). By contrast, most connected cells had somata at depths of 1400–1600 μm, where thalamic axons arborize in L5B/6A (7, 8), even though we sampled substantially from depths shallower than 1400 μm (Fig. 2J, left).…”

“…Recent quantitative measurements of reconstructed TC axons suggest, however, that innervation of L5/6 may be significant albeit less than that of L4 (8). Therefore, L5/6 neurons might integrate sensory information from at least two classes of inputs: the direct thalamocortical pathway and the indirect L4→L2/3→L5/6 pathway.…”

Juxtasomal Biocytin Labeling to Study the Structure-function Relationship of Individual Cortical Neurons

“…One example of such long-range projections are neurons from primary somatosensory cortex projecting to secondary somatosensory cortex or dysgranular zones thus projecting to areas which are several millimeters away from the labeling site 4,20 . When axonal projections of even larger dimensions are investigated (such as thalamocortical projections), survival time should be increased 15 . Important to realize is that electroporation of the neuron will have a profound effect on the physiological condition of the neuron due to excessive sodium influx from the electrode solution.…”

“…We are only beginning to understand cell type-specific functions across neuronal networks and much is still to be discovered. To this end, many labs are implementing experimental approaches that allow the analysis of morphological properties of the same neuronal population from which physiological parameters have been obtained 1,[10][11][12][13][14][15] . Here, we demonstrate the juxtasomal labeling technique 16,17 which involves electrophysiological recordings using conventional patch pipettes in the extracellular (thus noninvasive) configuration in combination with electroporation of the recorded neuron with biocytin.…”