Abstract
Early in auditory processing, neural responses faithfully reflect acoustic input. At higher stages of auditory processing, however, neurons become selective for particular call types, eventually leading to specialized regions of cortex that preferentially process calls at the highest auditory processing stages. We previously proposed that an intermediate step in how nonselective responses are transformed into call-selective responses is the detection of informative call features. But how neural selectivity for informative call features emerges from nonselective inputs, whether feature selectivity gradually emerges over the processing hierarchy, and how stimulus information is represented in nonselective and feature-selective populations remain open question. In this study, using unanesthetized guinea pigs (GPs), a highly vocal and social rodent, as an animal model, we characterized the neural representation of calls in 3 auditory processing stages-the thalamus (ventral medial geniculate body (vMGB)), and thalamorecipient (L4) and superficial layers (L2/3) of primary auditory cortex (A1). We found that neurons in vMGB and A1 L4 did not exhibit call-selective responses and responded throughout the call durations. However, A1 L2/3 neurons showed high call selectivity with about a third of neurons responding to only 1 or 2 call types. These A1 L2/3 neurons only responded to restricted portions of calls suggesting that they were highly selective for call features. Receptive fields of these A1 L2/3 neurons showed complex spectrotemporal structures that could underlie their high call feature selectivity. Information theoretic analysis revealed that in A1 L4, stimulus information was distributed over the population and was spread out over the call durations. In contrast, in A1 L2/3, individual neurons showed brief bursts of high stimulus-specific information and conveyed high levels of information per spike. These data demonstrate that a transformation in the neural representation of calls occurs between A1 L4 and A1 L2/3, leading to the emergence of a feature-based representation of calls in A1 L2/3. Our data thus suggest that observed cortical specializations for call processing emerge in A1 and set the stage for further mechanistic studies.
Highlights
Pure tone tuning bandwidths of tone-responsive neurons at all processing stages showed a dependence on best frequency (Fig 1G; ANCOVA with best frequency as covariate, p = 0.0071), and after controlling for this frequency dependence, the bandwidths of vMGB neurons were significantly higher than A1 L2/3 neurons (ANCOVA constrained to same slopes; intercept effect p = 0.0017; post hoc Tukey honestly significant difference (HSDA) vUM:GPBlevaesresnuosteAt1haLt4H: SpD=h0a.s0b5e3e,nAd1efLin2e/d3avsehrosunsesvtMlysGigBn:ipfic=a0n.t0d0if1f2er).eAnc1eLin4itasnfidrstmentionin A1 L2/3 bandwidths were not significantly different (p = 0.554)
Many previous studies have explored the neural representation of conspecific calls in subcortical and cortical areas across species [6,7,8,9,15,16,17,18,19,20,21,22,23,24,25,26,27,59], exactly where and how call selective responses emerge in the auditory processing hierarchy has remained unclear
Some studies have suggested that selectivity for ultrasonic vocalizations (USVs) in a manner not consistent with spectral content might arise at subcortical stations [5] and lead to an overrepresentation of USV-selective responses in the inferior colliculus (IC) [60]
Summary
We recorded the activity of single neurons located in the vMGB, A1 L4, and A1 L2/3 of unanesthetized, head-fixed, passively listening GPs (Fig 1A, top). Vocalization selectivity in the auditory cortex spectral energy across call types, many A1 L2/3 neurons responded to few call types and only in narrow windows, suggesting that they were likely driven by specific spectrotemporal features that occur during calls, consistent with our earlier theoretical model [29] We tested these hypotheses by estimating the spectrotemporal receptive fields (STRFs) that best explained neural responses across the processing stages. Vocalization selectivity in the auditory cortex stimulus-specific information (Fig 8J; p = 2.7 × 10−6, Kruskal–Wallis test; Dunn–Sidak post hoc test p-values are as follows: vMGB versus A1 L4: p = 0.021, A1 L2/3 versus vMGB: p = 1.3 × 10−6, A1 L2/3 versus A1 L4: p = 0.007) We confirmed that these results were consistent over a wide range of window sizes used for analysis (S1 Fig). FDR,AfUalse: Adinscaobvberyevriaatet;ioHnSlDis,thhoansebsetelynsciogmnifpicilaendtfdoirftfehroesnecue;sKed–iSn, TKaoblmleo1g:oPrloeva–sSemveirnifoyvt;hMatIa, mlleuntutraileisnaforremcoartiroenc;t: PSTH, peristimulus time histogram; STRF, spectrotemporal receptive field
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