Plasticity in the barrel cortex of the adult mouse: effects of chronic stimulation upon deoxyglucose uptake in the behaving animal

Abstract

We investigated experience-dependent regulation of neuronal activity in the whisker-to-barrel pathway of the adult mouse using the autoradiographic deoxyglucose (DG) method. Animals were placed in the Lausanne whisker stimulator, and three of their whisker follicles were passively stimulated for a period of 1, 2, or 4 d. After this period, mice received a dose of DG and were placed in a cage containing a pile of wooden sticks. Mice that underwent the same procedure except the passive stimulation served as controls. Patterns of stimulus-dependent DG uptake were studied in the somatosensory cortex and in the trigeminal sensory brainstem complex. DG uptake in the barrels corresponding to the passively stimulated whiskers was lower than in controls. This decrease was present throughout the radial extent of a barrel column and was observed in all passively stimulated animals. Quantitative analysis confirmed these observations and, furthermore, showed a statistically significant decrease in DG uptake in barrels neighboring the passively stimulated ones. In half of the animals, the brainstem nuclei showed a decreased DG uptake in the representation of the passively stimulated whiskers, whereas in the other animals the pattern of DG uptake was as in controls. We propose that the signs of cortical plasticity are due to a mechanism that operates in layer IV and functions as a gate for peripheral sensory activity to enter cortical circuitry.

Modified Sensory Processing in the Barrel Cortex of the Adult Mouse After Chronic Whisker Stimulation

“…In addition, we show that the depression of PW-evoked response is restricted to the "stimulated" barrel because responses in adjacent "nonstimulated" barrels C1 and D2 to their corresponding PW are not altered. These observations correlate well with the similarly localized decrease in deoxyglucose uptake described by Welker et al (1992). The depression of neuronal firing may be attributable to homeostatic downregulations of the cortical network to stabilize its own level of activity in response to a period of chronic increase in sensory drive.…”

“…Layer IV is the cortical entry of peripheral signals. In rodents, each barrel processes primarily sensory signals ascending from the corresponding whisker (Armstrong-James and Fox 1987;Simons 1978;Welker et al 1992), reflecting the segregation of TC-axonal branches from individual barreloids within the corresponding barrels (Arnold et al 2001;Bernardo and Woolsey 1987;Frost and Caviness 1980;Jensen and Killackey 1987;Killackey 1973). In mice and rats barrels contain glutamatergic neurons, mainly spiny stellate cells, and GABAergic inhibitory aspiny neurons (Harris and Woolsey 1983;Porter et al 2001;White 1978;White and Rock 1980).…”

“…It has been shown that a prolonged period of chronic whisker stimulation in a normally behaving adult mouse induces functional and morphological changes in the corresponding barrel (Knott et al 2002;Rocamora et al 1996;Welker et al 1989Welker et al , 1992. An electron microscopical analysis demonstrated that a 24-h period of chronic whisker stimulation causes a fourfold increase in the density of spineous GABAergic synapses in the stimulated barrel.…”

Plasticity in primary somatosensory cortex resulting from environmentally enriched stimulation and sensory discrimination training

“…Stimulation per se is inadequate. When appropriate conditions of behavioral context are not met, no change, or even negative changes, may be the result (Welker et al, 1992;Polley, 2004). These findings substantially differ from the changes produced by behaviorally relevant stimulation versus deprivation in our study (See Figure 3).…”

Ipsilateral Whiskers Suppress Experience-Dependent Plasticity in the Barrel Cortex

“…For example, Polley et al (1999) showed that the cortical area activated by whisker deflection actually shrinks after exposure to a sensoryrich environment in which animals are encouraged to use the whiskers. Second, passive whisker overstimulation of a single whisker leads to reduced 2-deoxyglucose uptake in the corresponding barrel columns (Welker et al, 1992).…”