Integrating information from different senses in the auditory cortex

Abstract

Multisensory integration was once thought to be the domain of brain areas high in the cortical hierarchy, with early sensory cortical fields devoted to unisensory processing of inputs from their given set of sensory receptors. More recently, a wealth of evidence documenting visual and somatosensory responses in auditory cortex, even as early as the primary fields, has changed this view of cortical processing. These multisensory inputs may serve to enhance responses to sounds that are accompanied by other sensory cues, effectively making them easier to hear, but may also act more selectively to shape the receptive field properties of auditory cortical neurons to the location or identity of these events. We discuss the new, converging evidence that multiplexing of neural signals may play a key role in informatively encoding and integrating signals in auditory cortex across multiple sensory modalities. We highlight some of the many open research questions that exist about the neural mechanisms that give rise to multisensory integration in auditory cortex, which should be addressed in future experimental and theoretical studies.

Fig. 1

Multisensory spatial receptive fields of a ferret auditory cortical neuron. The raster plots in the 3 left panels show the action potential responses of the neuron to 100 ms bursts of broadband noise (far left plot), a white light-emitting diode (center raster plot), or both the sound and light together (right raster plot). In each raster plot, the timing of stimuli are indicated by a horizontal bar at the bottom of the plot, and responses to stimuli are plotted across a range of stimulus locations in the horizontal plane (y-axis). The spike rate functions of the neuron for auditory (blue line), visual (green line), and audiovisual (red line) stimulation are summarized in the plot to the far right. In this example, pairing spatially coincident visual and auditory stimuli resulted in a more sharply tuned spatial response profile that carried significantly more information about stimulus location. Adapted from Bizley and King (2008).

Fig. 2

Schematic of auditory cortex in the ferret, showing organization of visual inputs. Auditory cortical areas are located on the anterior, middle and posterior ectosylvian gyri (AEG, MEG and PEG). Other abbreviations: PPc, caudal posterior parietal cortex; SSY, suprasylvian cortex; V1, primary visual cortex; V2, secondary visual cortex; sss, suprasylvian sulcus; pss, pseudosylvian sulcus; D, dorsal; R, rostral.

Fig. 3

Cartoons of 2 forms of spectral multiplexing observed in auditory cortex. a. Phase-of-firing multiplexing described by Kayser et al. (2009b). LFPs have been categorized into four phases, represented in color. The pattern of action potentials (top row) or local field potential (LFP) phase (middle row) alone do not provide as much information about auditory stimuli as the timing of action potentials with respect to the LFP phase in which they occur (bottom row). b. Phase-based-enhancement of spiking responses described by Lakatos et al. (2007). A somatosensory stimulus (hand, bottom row) resets the phase of the LFP (top row) in auditory cortex, but does not result in significant spiking activity (middle row). Spiking responses to subsequent auditory stimulation (ears, bottom row) are suppressed during troughs and enhanced during peaks of the ongoing LFP.

Fig. 4

Time-division multiplexing within a single auditory cortex neuron described by Walker et al. (2011). a. Post-stimulus time histogram, showing the mean firing rate of the neuron across all presentations of an artificial vowel sound presented over 4 locations in horizontal space, 4 values of the fundamental frequency (“pitch”), and 4 spectral identities (“timbre”). Sound presentation time is indicated by the black horizontal bar below the plot. b. Mutual Information carried by the neuron for either the timbre (black line) or pitch (red line) of the sound throughout its response. Note that these values peak at different time points.

Fig. 5

Schematic of excitatory and inhibitory summation to achieve delayed temporal integration of excitatory signals. The target neuron (above, “Σ”) receives input from an early inhibitory interneuron (black, “−”) and both an early and late excitatory input (white, “+”), the result of which is integration of excitatory signals in the later time window only.