Subthreshold auditory inputs to extrastriate visual neurons are responsive to parametric changes in stimulus quality: sensory-specific versus non-specific coding

Abstract

A new subthreshold form of multisensory processing has been recently identified that results from the convergence of suprathreshold excitatory inputs from one modality with subthreshold inputs from another. Because of the subthreshold nature of the second modality, descriptive measures of sensory features such as receptive field properties or location are not directly apparent as they are for traditional bimodal neurons. This raises the question of whether or not subthreshold signals actually convey sensory-specific receptive field information as seen in their bimodal counterparts, or if they represent non-specific effects such as arousal. The present experiment addressed this issue in visually-responsive neurons from the cat posterolateral lateral suprasylvian cortex (PLLS). Single-unit electrophysiological techniques were used to record neuronal responses to visual, auditory and combined visual-auditory stimuli while the intensity of stimulation in the subthreshold auditory modality was systematically altered. The results showed that subthreshold multisensory neurons were sensitive to changes in auditory stimulus intensity. These receptive field sensitivities are similar to those observed in bimodal neurons and thereby represent sensory-specific, not arousal-related responses. In addition, these results provide further support for the notion that multisensory processing occurs along a dynamic continuum of neuronal convergence patterns from bimodal to purely sensory-specific.

Figure 1

Location of recording penetrations in posterolateral lateral suprasylvian (PLLS) visual area of the cat cortex. The schematic of the lateral view of cat cortex shows the anterior-posterior level corresponding to the 3 coronal sections (A-C). The coronal sections reveal the location of the PLLS area (shaded grey) and the 4 recording penetrations (grey lines). The thick, black arrows indicate the lateral suprasylvian sulcus.

Figure 2

Changes in the intensity of auditory stimulation resulted in concomitant response changes for a representative subthreshold multisensory neuron. As indicated by the response rasters and histograms, this PLLS neuron showed a strong response to a visual stimulus (V=9.8±4.5 mean spikes/trial ± standard deviation), but not to the auditory stimulus presented alone (A81dB). When auditory stimuli of different preset intensities (66, 75 or 81dB) were presented in combination with the visual stimulus, the response was increased for each stimulus pair (VA66dB=11.4±3.9; VA75dB=13.5±4.5; VA81dB=13.0±4.8) and was significantly facilitated (‘*’, P<0.05) at the louder intensities (VA75dB, VA81dB). The bar graph summarizes these incremental response changes correlated with progressive changes of intensity of the stimulus. Mean spontaneous activity = Sp.

Figure 3

Responses of subthreshold multisensory neurons to combined stimuli (VA; y-axis) were consistently greater than the responses to the visual stimuli alone (V; x-axis); hence, they plotted above the line of unity (dashed). A separate plot is presented for each of the auditory stimulus intensity conditions, where it can be seen that the slope of the fitted lines (solid) increased progressively with increases in the intensity of the auditory stimulus (VA66dB slope=1.19; VA75dB slope=1.22; VA81dB slope=1.26).

Figure 4

Average response levels (mean spikes/trial ± standard error of the mean) for the population of subthreshold multisensory neurons (n=45) to visual stimulation alone (V=9.7±1.1) were significantly (‘*’, P<0.05) and incrementally facilitated by the presence of progressively louder auditory stimuli (VA66dB=12.1±1.3; VA75dB=12.7±1.2; VA81dB=12.8±1.3). Furthermore, not only did the loudest auditory combination (VA81dB) produce the strongest average response as well as the largest response change, it was also statistically greater (‘†’, P<0.05) than the combined response involving the lowest auditory stimulus (VA81dB>VA66dB).