Sensory Input Directs Spatial and Temporal Plasticity in Primary Auditory Cortex

Abstract

The cortical representation of the sensory environment is continuously modified by experience. Changes in spatial (receptive field) and temporal response properties of cortical neurons underlie many forms of natural learning. The scale and direction of these changes appear to be determined by specific features of the behavioral tasks that evoke cortical plasticity. The neural mechanisms responsible for this differential plasticity remain unclear partly because important sensory and cognitive parameters differ among these tasks. In this report, we demonstrate that differential sensory experience directs differential plasticity using a single paradigm that eliminates the task-specific variables that have confounded direct comparison of previous studies. Electrical activation of the basal forebrain (BF) was used to gate cortical plasticity mechanisms. The auditory stimulus paired with BF stimulation was systematically varied to determine how several basic features of the sensory input direct plasticity in primary auditory cortex (A1) of adult rats. The distributed cortical response was reconstructed from a dense sampling of A1 neurons after 4 wk of BF-sound pairing. We have previously used this method to show that when a tone is paired with BF activation, the region of the cortical map responding to that tone frequency is specifically expanded. In this report, we demonstrate that receptive-field size is determined by features of the stimulus paired with BF activation. Specifically, receptive fields were narrowed or broadened as a systematic function of both carrier-frequency variability and the temporal modulation rate of paired acoustic stimuli. For example, the mean bandwidth of A1 neurons was increased (+60%) after pairing BF stimulation with a rapid train of tones and decreased (-25%) after pairing unmodulated tones of different frequencies. These effects are consistent with previous reports of receptive-field plasticity evoked by natural learning. The maximum cortical following rate and minimum response latency were also modified as a function of stimulus modulation rate and carrier-frequency variability. The cortical response to a rapid train of tones was nearly doubled if BF stimulation was paired with rapid trains of random carrier frequency, while no following rate plasticity was observed if a single carrier frequency was used. Finally, we observed significant increases in response strength and total area of functionally defined A1 following BF activation paired with certain classes of stimuli and not others. These results indicate that the degree and direction of cortical plasticity of temporal and receptive-field selectivity are specified by the structure and schedule of inputs that co-occur with basal forebrain activation and suggest that the rules of cortical plasticity do not operate on each elemental stimulus feature independently of others.

Spectral integration plasticity in cat auditory cortex induced by perceptual training

“…The literature is currently divided between studies demonstrating that receptive field plasticity in AI is dictated by stimulus input statistics under conditions of varying (Polley et al, 2004) or absent (Kilgard et al, 2001) task demands and studies that demonstrate that AI receptive field plasticity is relatively independent of stimulus statistics, but instead is guided by the demands of the conditioning task (Polley et al, 2006). The present results most strongly support findings that receptive field reorganization is directed by statistics of sensory inputs paired with behavioral reinforcement.…”

Neuromagnetic evidence of broader auditory cortical tuning in schizophrenia

“…Cortical tuning is dynamic and can be rapidly altered by experience (Kilgard et al, 2001, Recanzone et al, 1993. Experience-dependent plasticity in auditory responses is found even in averaged evoked responses from human MEG recordings (Cansino andWilliamson, 1997, Pantev andLutkenhoner, 2000).…”

Asynchronous inputs alter excitability, spike timing, and topography in primary auditory cortex

“…In contrast, decreasing input correlation via strabismus, monocular deprivation, or frequency discrimination training results in prolonged latencies in the visual and auditory cortices (Chino et al, 1988;Chino et al, 1983;Eschweiler and Rauschecker, 1993;Recanzone et al, 1993). Decreased response latencies were observed after a single tone was paired with nucleus basalis stimulation, while latencies were increased when seven different tones were independently paired with nucleus basalis stimulation (Kilgard et al, 2001a). In that study, we speculated that latency was decreased when map expansion drove a net increase in the correlated activity across A1 and latency was increased when tonal inputs were distributed across A1 in the absence of map plasticity.…”

“…Experiments conducted in the visual, somatosensory, and auditory systems have provided compelling evidence that different sensory input patterns can lead to distinctly different forms of cortical reorganization (Allard et al, 1991;Stryker and Strickland, 1984;Wang et al, 1995). Behaviorally relevant sensory and motor events are marked by increased activity in nucleus basalis (NB), which projects to the entire cortex and powerfully modulates plasticity (Conner et al, 2003;Kilgard and Merzenich, 1998b;Kilgard et al, 2001a;Weinberger, 1998).…”

“…These tones were paired with electrical activation of the nucleus basalis as in our earlier studies. Nucleus basalis stimulation paired with sensory input has been used extensively by several research groups to promote input guided cortical plasticity in the absence of behavior (Bakin and Weinberger, 1996;Edeline et al, 1994;Kilgard et al, 2001a;Metherate and Ashe, 1993;Rasmusson and Dykes, 1988). While nucleus basalis stimulation is an unnatural method for gating representational plasticity, this paradigm makes it possible to manipulate sensory statistics by delivering arbitrary input patterns without the need for time-consuming behavioral training or surgical procedures.…”