Right–left asymmetry in the cortical processing of sounds for social communication vs. navigation in mustached bats

Abstract

In the Doppler-shifted constant frequency processing area in the primary auditory cortex of mustached bats, Pteronotus parnellii, neurons respond to both social calls and to echolocation signals. This multifunctional nature of cortical neurons creates a paradox for simultaneous processing of two behaviorally distinct categories of sound. To test the possibility of a stimulus-specific hemispheric bias, single-unit responses were obtained to both types of sounds, calls and pulse-echo tone pairs, from the right and left auditory cortex. Neurons on the left exhibited only slightly higher peak response magnitudes for their respective best calls, but they showed a significantly higher sensitivity (lower response thresholds) to calls than neurons on the right. On average, call-to-tone response ratios were significantly higher for neurons on the left than for those on the right. Neurons on the right responded significantly more strongly to pulse-echo tone pairs than those on the left. Overall, neurons in males responded to pulse-echo tone pairs with a much higher spike count compared to females, but this difference was less pronounced for calls. Multidimensional scaling of call responses yielded a segregated representation of call types only on the left. These data establish for the first time, a behaviorally directed right-left asymmetry at the level of single cortical neurons. It is proposed that a lateralized cortex emerges from multiparametric integration (e.g. combination-sensitivity) within a neuron and inhibitory interactions between neurons that come into play during the processing of complex sounds.

Right ear advantage for vocal communication in frogs results from both structural asymmetry and attention modulation

“…Since projections to the midbrain arise primarily from the contralateral auditory periphery, the results obtained here support the hypothesis that right-ear/left-hemispheric superiority for processing communication sounds in frogs is to a significant extent due to structural asymmetries in the way the auditory system processes information. This finding is also in agreement with earlier studies on REA in amniote vertebrates holding a left-hemisphere priority for processing conspecific/neighbor vocalizations [1,[16][17][18][19]24,[52][53][54][55][56][57]. Furthermore, the REA in music frogs has been demonstrated, at least in part, in a preliminary behavioral study using a head orienting task in which the subjects preferentially turned their bodies toward the right while listening to HSA playbacks, but did not show a turning preference in silence (unpublished data).…”

“…For non-human animals, left-hemispheric dominance for conspecific communication sounds has been reported in non-human primates [19,[53][54][55]59], other mammals [16,17,24,56,57], birds [60,61] and frogs [10]. Interestingly, communication asymmetry has been reported in bats at the level of single cortical neurons, with left-hemispheric neuronal advantage for processing social calls and right-hemispheric neuronal advantage in processing navigational signals [24]. These findings including the present results suggest a phylogenetically early emergence of vocal communication asymmetries [4].…”

“…To explain the observed hemispheric auditory asymmetry, various models have been proposed, including those based on the temporal and spectral structures of communication sounds [20], on an attentional filter termed the double-filtering-by-frequency model [21] and on different temporal integration windows for each hemisphere termed the asymmetric-sampling-in-time model [22,23]. Multiparametric integration and lateral inhibition at level of the neural network may also be involved in auditory asymmetry, as exemplified by neuronal responses in bats [24]. Most frequently, however, REA has been explained by a structural model and/or an attentional model, corresponding to bottom-up and top-down processing, respectively [25,26].…”

Asymmetric neural coding revealed by in vivo calcium imaging in the honey bee brain

“…Using three alcohols and one binary mixture as odourants, we found that odour processing is asymmetric: the neural odour representations were more separated in the right AL, and bees with only their right antenna in use were better in segregating a target odour from a background odour in a cross-adaptation experiment. Similarly, in vertebrates the discriminatory power of sensory representations can be lateralized, as has been shown in the visual system of birds [27][28][29][30][31] both behaviourally and physiologically (fMRI during a discrimination task described in [31], electrophysiological recordings in the primary auditory area in [30] and in the auditory system of bats [32]; the latter was revealed by measuring inter-stimuli Euclidean distances).…”

The biological significance of acoustic stimuli determines ear preference in the music frog

“…Lesions of the left hemisphere reduce the ability to discriminate and/or produce conspecific sounds to a greater degree than lesions of the right hemisphere. Neurophysiological studies in bats have shown that the left hemisphere neurons are more responsive to social calls while those of the right are more responsive to navigational signals (Kanwal, 2012). Theoretically, neural lateralization would improve information processing efficiency by providing specialized analysis within each hemisphere, thereby enhancing the ability of land vertebrates to make critical decisions related to mating or feeding in dangerous environments (Rogers et al, 2004).…”