Auditory cortex of bats and primates: managing species-specific calls for social communication

Abstract

Individuals of many animal species communicate with each other using sounds or "calls" that are made up of basic acoustic patterns and their combinations. We are interested in questions about the processing of communication calls and their representation within the mammalian auditory cortex. Our studies compare in particular two species for which a large body of data has accumulated: the mustached bat and the rhesus monkey. We conclude that the brains of both species share a number of functional and organizational principles, which differ only in the extent to which and how they are implemented. For instance, neurons in both species use "combination-sensitivity" (nonlinear spectral and temporal integration of stimulus components) as a basic mechanism to enable exquisite sensitivity to and selectivity for particular call types. Whereas combination-sensitivity is already found abundantly at the primary auditory cortical and also at subcortical levels in bats, it becomes prevalent only at the level of the lateral belt in the secondary auditory cortex of monkeys. A parallel-hierarchical framework for processing complex sounds up to the level of the auditory cortex in bats and an organization into parallel-hierarchical, cortico-cortical auditory processing streams in monkeys is another common principle. Response specialization of neurons seems to be more pronounced in bats than in monkeys, whereas a functional specialization into "what" and "where" streams in the cerebral cortex is more pronounced in monkeys than in bats. These differences, in part, are due to the increased number and larger size of auditory areas in the parietal and frontal cortex in primates. Accordingly, the computational prowess of neural networks and the functional hierarchy resulting in specializations is established early and accelerated across brain regions in bats. The principles proposed here for the neural "management" of species-specific calls in bats and primates can be tested by studying the details of call processing in additional species. Also, computational modeling in conjunction with coordinated studies in bats and monkeys can help to clarify the fundamental question of perceptual invariance (or "constancy") in call recognition, which has obvious relevance for understanding speech perception and its disorders in humans.

Figure 1

A. Amplitude envelopes (above) and spectrograms (below) of five examples of simple syllabic calls emitted by mustached bats (P. parnellii). B. Amplitude envelopes (above) and spectrograms (below) of calls emitted by rhesus monkeys. C. Speech sounds for a phoneme, /da/ and simple words.

Figure 2

Spectrographic examples of communication calls showing several variants of a simple syllable, sinusoidal FM (sFM), emitted by mustached bats (A) and the archscream call emitted by rhesus monkeys (B).

Figure 3

A. Organization of the AC in rhesus monkeys showing the reversal of tonotopic mappings in the core, belt and parabelt areas. Organization of the AC in the mustached bats. B. Lateral view of the bat’s brain showing the functionally defined subdivisions of the AC in mustached bats. The primary auditory cortex (AI) is shown as cross-hatched. ‘a’ AI-anterior, ‘b’ AI-posterior, ‘c’ DSCF area (shown in gray), ‘d’ CF/CF area (fine stippled) ‘e’ DIF area, ‘f’ FM-FM area (coarse stippled), ‘g’ DF area, ‘h’ VF area, ‘i’ DM area, ‘j’ TE area, ‘k’ H1-H2 area, ‘l’ VA area, ‘m’ VP area (adapted from Suga et al., 1987, (78). Detailed representation of the FM-FM, CF/CF, DSCF and AIp areas in the AC. The DSCF area occupies nearly 30% of the area of the tonotopically organized primary AC and represents a small range (60.6 to 62.3 kHz) of frequencies.

Figure 4

A. Dot raster and PSTH plots to show the neural response to whole calls in the A1 of mustached bats (A) and rhesus monkeys (B). Response patterns in both species are generally similar and show a phasic response onset with a clear peak firing rate that lasts for a few ms. Response duration is an order of magnitude longer in primates compared to bats. Bin width = 5 ms.

Figure 5

Dot raster (above) and PSTH plots (below) to demonstrate combination-sensitivity in the firing rate of a neuron by presentation of spectrographic components in the call response of neurons (A) in the DSCF area in mustached bats and (B) in a neuron in the belt region of the rhesus monkey AC. Bin width = 5 ms.

Figure 6

A. Hypothetical scheme showing the steps for parallel-hierarchical processing of communication calls along a subcortical “what” stream in mustached bats. The scheme is based on what we know about processing of echolocation signals in the mustached bat’s auditory system (68). B. Flow-chart showing the parallel-hierarchical processing of auditory information and the origin of the “what” and “where” streams in the brain of rhesus monkeys. DCN, dorsal cochlear nucleus, VCN, ventral cochlear nucleus, ICx, external nucleus of the inferior colliculus; ICc, central nucleus of the inferior colliculus; MGm, MGv, MGd, medial, ventral and dorsal divisions, respectively, of the medial geniculate body; bDFM, bent downward FM; bUFM, bent upward FM; dRFM, descending rippled FM; fSFM, fixed sinusoidal FM; QCFl, long quasi CF; QCFs, short quasi CF.

Figure 7

Neural responses (PSTHs above and dot rasters below) showing preference for upward versus downward frequency modulated sweeps in (A) the DSCF area in mustached bats (95), and (B) the rhesus monkey auditory cortex. Responses in the rhesus monkey also show a tuning to the slope of the upward FM. Bin width = 5 ms.

Figure 8

A and B. Bar graphs for the peak firing rate of two single neuron responses in the DSCF area in mustached bats showing both invariance and variation of responses to different amplitudes of simple syllabic call types (1 to 14). C. Bar graphs of responses of a cortical neuron to 14 syllables and their variants. Variants are produced by shifting the fundamental frequency and harmonic spectrum of the waveform by ±1, ±2, and ±3 standard deviation (s.d.) from the mean of the natural variation in call types. Neuron responds with different response magnitudes to several variants of the same syllable type. Neural response invariance possibly underlies the phenomenon of perceptual invariance, but appears to be absent in the AC. Each stimulus presentation was repeated 10 times. Bin width = 10 ms.

Figure 9

Functional organization of the “what” (pink) and “where” (green) cortical processing streams in (A) primates, and (B) as hypothesized for mustached bats. The bat model is divided into a core system for auditory analysis of echoes and calls and an extended system for the processing of meaning gleaned from echoes and calls. aFAF and pFAF, anterior and posterior frontal auditory fields,; MGd and MGv, dorsal and ventral medial geniculate nuclei; SGn, suprageniculate nucleus; Numbers refer to Brodmann areas.