Auditory motion does not modulate spiking activity in the middle temporal and medial superior temporal visual areas

Abstract

The integration of multiple sensory modalities is a key aspect of brain function, allowing animals to take advantage of concurrent sources of information to make more accurate perceptual judgments. For many years, multisensory integration in the cerebral cortex was deemed to occur only in high-level "polysensory" association areas. However, more recent studies have suggested that cross-modal stimulation can also influence neural activity in areas traditionally considered to be unimodal. In particular, several human neuroimaging studies have reported that extrastriate areas involved in visual motion perception are also activated by auditory motion, and may integrate audiovisual motion cues. However, the exact nature and extent of the effects of auditory motion on the visual cortex have not been studied at the single neuron level. We recorded the spiking activity of neurons in the middle temporal (MT) and medial superior temporal (MST) areas of anesthetized marmoset monkeys upon presentation of unimodal stimuli (moving auditory or visual patterns), as well as bimodal stimuli (concurrent audiovisual motion). Despite robust, direction selective responses to visual motion, none of the sampled neurons responded to auditory motion stimuli. Moreover, concurrent moving auditory stimuli had no significant effect on the ability of single MT and MST neurons, or populations of simultaneously recorded neurons, to discriminate the direction of motion of visual stimuli (moving random dot patterns with varying levels of motion noise). Our findings do not support the hypothesis that direct interactions between MT, MST and areas low in the hierarchy of auditory areas underlie audiovisual motion integration.

Unidirectional monosynaptic connections from auditory areas to the primary visual cortex in the marmoset monkey

“…Considering the relatively slow conduction of the visual pathway, and the fact that visual response latencies increase further when stimuli have low visibility (Bourne et al 2002 ; Lui et al 2012 ), a reciprocal projection from V1 to auditory areas would not provide a similar processing advantage. A sparse projection from caudal auditory cortex to area MT (Palmer and Rosa 2006a ) has been hypothesised to facilitate processing of visual motion, but recent single-neuron recording studies have not been able to confirm the existence of such an effect (Chaplin et al 2018a , b ).…”

Auditory and Visual Motion Processing and Integration in the Primate Cerebral Cortex

“…The neural representation of auditory motion does not necessarily have to be located in purely auditory regions. Direct reciprocal connections between MT/MST and the auditory cortex have been identified in primates (Palmer and Rosa, 2006 ), and two recent electrophysiological studies (Chaplin et al, 2018 ; Kafaligonul et al, 2018 ) have reported evoked potentials in areas MT/MST in response to stationary auditory clicks. Two human imaging studies have reported that the hMT+ complex responds to auditory motion (Poirier et al, 2005 ; Strnad et al, 2013 ), but it has also been argued that observed auditory responses in hMT+ could be explained by localization errors (Jiang et al, 2014 ), and no study has found any evidence for spiking activity in response to auditory stimuli (moving or stationary) in the monkey MT complex.…”

“…A number of imaging studies have also found that audiovisual stimulation produces distinct activation (compared to visual only stimulation) in hMT+ (Alink et al, 2008 ; Lewis and Noppeney, 2010 ; Strnad et al, 2013 ; von Saldern and Noppeney, 2013 ), suggesting that auditory stimuli can modulate visually evoked responses (although this is not always the case, e.g., Wuerger et al, 2012 ). These regions receive sparse inputs from auditory cortex (Palmer and Rosa, 2006 ), and show evoked potentials in response to auditory stimuli (Chaplin et al, 2018 ; Kafaligonul et al, 2018 ). Additionally, auditory motion has been shown to affect various aspects of visual perception, such as improving visual motion detection (Kim et al, 2012 ), improve learning in visual motion tasks (Seitz et al, 2006 ), and induce visual illusions (Sekuler et al, 1997 ; Meyer and Wuerger, 2001 ; Kitagawa and Ichihara, 2002 ; Beer and Röder, 2004 ; Soto-Faraco et al, 2005 ; Freeman and Driver, 2008 ; Alink et al, 2012a ; Kafaligonul and Stoner, 2012 ; Kafaligonul and Oluk, 2015 ).…”

“…To specifically test this hypothesis, we have investigated if auditory motion cues are integrated with visual motion cues in MT/MST, by recording spiking activity and characterizing the ability of neurons to encode the direction of motion, using ideal observer analysis (Chaplin et al, 2018 ). We presented random dot patterns that moved either leftwards or rightwards, and manipulated the strength of the visual motion signal by reducing the coherence of the dots (i.e., making some proportion of the dots move in random directions).…”

“…(B) Neurometric performance (measured as the area under the receiver operating characteristic (ROC) curve, Britten et al, 1992 , which corresponds to the performance of an ideal observer discriminating the direction of motion using the spiking activity of the neuron) of a marmoset MT neuron when discriminating leftwards and rightwards motion under visual (blue) and audiovisual (red) conditions at different levels of motion coherence (strength of motion signal). The addition of the auditory stimulus did not shift the neurometric curve to the left as would be expected if the neuron was integrating the auditory motion cue (adapted from Chaplin et al, 2018 ).…”