Auditory influences on non-auditory cortices

Abstract

Although responses to auditory stimuli have been extensively examined in the well-known regions of auditory cortex, there are numerous reports of acoustic sensitivity in cortical areas that are dominated by other sensory modalities. Whether in 'polysensory' cortex or in visual or somatosensory regions, auditory responses in non-auditory cortex have been described largely in terms of auditory processing. This review takes a different perspective that auditory responses in non-auditory cortex, either through multisensory subthreshold or bimodal processing, provide subtle but consistent expansion of the range of activity of the dominant modality within a given area. Thus, the features of these acoustic responses may have more to do with the subtle adjustment of response gain within a given non-auditory region than the encoding of their tonal properties.

Figure 1. Auditory influences on visual activity in the anterior ectosylvian visual area (AEV)

Part ‘A’ illustrates, on the lateral view of the cat cerebral cortex, the location of the AEV, as well as its position (shaded gray on coronal sections) within the ventral bank of the anterior ectosylvian sulcus. The line/black dot represent the recording penetration and site (respectively) of a bimodal (B) and a subthreshold multisensory (C) neuron, whose activity is depicted in subsequent parts. Part ‘B’ shows the activity (raster 1 dot=1 spike; histogram=10ms time bins) of an AEV bimodal neuron to a visual (ramp labeled ‘V’), auditory (square wave labeled ‘A’) and combined visual-auditory stimulation. The scatter plot in ‘B’ shows, for the population of AEV bimodal neurons, the relationship of activity elicited by visual stimulation alone (x-axis) versus that evoked by the combined visual-auditory stimuli (y-axis). Most bimodal AEV neurons exhibited combined responses that plotted above the line of unity, although the magnitude of these responses was generally small (<±50%; B: bar graph). Part ‘C’ shows the excitatory response of an AEV subthreshold multisensory neuron to a visual, and no response to the auditory stimulus. However, when the stimuli were combined, the resulting response was significantly (p<0.05, paired t-test) greater than that elicited by the visual stimulus alone. The scatter plot in ‘C’ for the population of AEV subthreshold multisensory neurons shows the relationship of activity elicited by visual stimulation alone (x-axis) versus that evoked by the combined visual-auditory stimuli (y-axis): most plotted above the line of unity. The magnitude of these responses was generally small (<±50%; C: bar graph).

Figure 2. Auditory influences on somatosensory activity in the rostral suprasylvian sulcus (RSS)

Part ‘A’ illustrates, on the lateral view of the cat cerebral cortex, the location of the RSS, as well as its position (shaded gray on coronal sections) within the lateral bank of the rostral suprasylvian ectosylvian sulcus. The line/black dot represent the recording penetration and site (respectively) of a bimodal (B) and a subthreshold multisensory (C) neuron whose activity is depicted in subsequent parts. Part ‘B’ shows the activity of an RSS bimodal neuron to a tactile (ramp labeled ‘T’), auditory (square wave labeled ‘A’) and combined tactile-auditory stimulation. The scatter plot in ‘B’ shows, for the population of bimodal neurons, the relationship of activity elicited by tactile stimulation alone (x-axis) versus that evoked by the combined tactile-auditory stimuli (y-axis). The large majority of bimodal RSS neurons exhibited combined responses that plotted above the line of unity; although the magnitude of these responses was generally small (B: bar graph), several examples >100% response change were observed. Part ‘C’ shows the excitatory response of an RSS subthreshold multisensory neuron to a tactile, but no response to an auditory stimulus. However, when the stimuli were combined, the resulting response was significantly (p<0.05, paired t-test) different than that elicited by the tactile stimulus alone. The scatter plot (C) for the population of RSS subthreshold multisensory neurons shows the relationship of activity elicited by tactile stimulation alone (x-axis) versus that evoked by the combined tactile-auditory stimuli (y-axis). This result consistently plotted away from the line of unity and represented response magnitudes that often exceeded 50%, as displayed in the bar graph in ‘C.’

Figure 3. Auditory influences on visual activity in the posterolateral lateral suprasylvian visual area (PLLS)

Part ‘A’ illustrates, on the lateral view of the cat cerebral cortex, the location of the PLLS, as well as its position (shaded gray on coronal sections) within the lateral bank of the suprasylvian sulcus. The line/black dot represent the recording penetration and site (respectively) of a bimodal (B) and a subthreshold multisensory (C) neuron whose activity is depicted in subsequent parts. Part ‘B’ shows the activity (raster of an PLLS bimodal neuron to a visual (ramp labeled ‘V’), auditory (square wave labeled ‘A’) and combined visual-auditory stimulation. The scatter plot in ‘B’ shows, for the population of bimodal neurons, the relationship of activity elicited by visual stimulation alone (x-axis) versus that evoked by the combined visual-auditory stimuli (y-axis). The large majority of bimodal neurons exhibited combined responses that plotted above the line of unity and, although the magnitude of these responses was generally small (B: bar graph) several responses were near or exceeded 100%. Part ‘C’ shows the excitatory response of an PLLS subthreshold multisensory neuron to a visual, but no response to an auditory stimulus. However, when the stimuli were combined, the resulting response was significantly (p<0.05, paired t-test) greater than that elicited by the visual stimulus alone. The scatter plot in ‘C’ for the population of PLLS subthreshold multisensory neurons shows the relationship of activity elicited by visual stimulation alone (x-axis) versus that evoked by the combined visual-auditory stimuli (y-axis): all plotted above the line of unity but the magnitude of these responses was generally small (<±50%; C: bar graph).

Figure 4. Auditory influences on visual activity in ferret visual Area 21

Part ‘A’ illustrates, on the lateral view of the ferret cerebral cortex, the location of the visual fields including Area 21, as well as the position of Area 21 (shaded gray on coronal sections) surrounding the posterior aspects of the lateral sulcus. The line/black dot represent the recording penetration and site (respectively) of neurons whose activity is depicted in subsequent parts. Part ‘B’ shows the activity (raster 1 dot=1 spike; histogram=10ms time bins) of an Area 21 neuron in response to a visual (ramp labeled ‘V’), but not to an auditory (square wave labeled ‘A’) stimulus; combined visual-auditory stimulation did not elicit a significant response change. The scatter plot in ‘B’ for the population of Area 21 neurons shows the relationship of activity elicited by visual stimulation alone (x-axis) versus that evoked by the combined visual-auditory stimuli (y-axis). Nearly all neurons had responses that plotted close to the line of unity (48% above, 52% below), and the average response of the population was unchanged between the visual only and the visual-auditory stimulus conditions. Part ‘C’ shows an Area 21 neuron that was responsive to visual stimulation, but not auditory and, when the stimuli were combined, there was a modest reduction in response. However, when the same neuron was tested in the presence of the inhibitory transmitter antagonist Bicuculline methiodide (thick black bar), the response to the combined visual-auditory stimulus was significantly greater than that elicited by the visual stimulus alone The blockade of inhibition had a similar effect on the population of Area 21 neurons, where the responses of most neurons now plotted above the line of unity (C: scatter plot) and the average spikes per trial significantly (C: bar graph; *= p<005) increased in the combined versus visual-only condition.