Coding of communication calls in the subcortical and cortical structures of the auditory system

The processing of species-specific communication signals in the auditory system represents an important aspect of animal behavior and is crucial for its social interactions, reproduction, and survival. In this article the neuronal mechanisms underlying the processing of communication signals in the higher centers of the auditory system--inferior colliculus (IC), medial geniculate body (MGB) and auditory cortex (AC)--are reviewed, with particular attention to the guinea pig. The selectivity of neuronal responses for individual calls in these auditory centers in the guinea pig is usually low--most neurons respond to calls as well as to artificial sounds; the coding of complex sounds in the central auditory nuclei is apparently based on the representation of temporal and spectral features of acoustical stimuli in neural networks. Neuronal response patterns in the IC reliably match the sound envelope for calls characterized by one or more short impulses, but do not exactly fit the envelope for long calls. Also, the main spectral peaks are represented by neuronal firing rates in the IC. In comparison to the IC, response patterns in the MGB and AC demonstrate a less precise representation of the sound envelope, especially in the case of longer calls. The spectral representation is worse in the case of low-frequency calls, but not in the case of broad-band calls. The emotional content of the call may influence neuronal responses in the auditory pathway, which can be demonstrated by stimulation with time-reversed calls or by measurements performed under different levels of anesthesia. The investigation of the principles of the neural coding of species-specific vocalizations offers some keys for understanding the neural mechanisms underlying human speech perception.     

Processing of Communication Calls in Guinea Pig Auditory Cortex

Vocal communication is an important aspect of guinea pig behaviour and a large contributor to their acoustic environment. We postulated that some cortical areas have distinctive roles in processing conspecific calls. In order to test this hypothesis we presented exemplars from all ten of their main adult vocalizations to urethane anesthetised animals while recording from each of the eight areas of the auditory cortex. We demonstrate that the primary area (AI) and three adjacent auditory belt areas contain many units that give isomorphic responses to vocalizations. These are the ventrorostral belt (VRB), the transitional belt area (T) that is ventral to AI and the small area (area S) that is rostral to AI. Area VRB has a denser representation of cells that are better at discriminating among calls by using either a rate code or a temporal code than any other area. Furthermore, 10% of VRB cells responded to communication calls but did not respond to stimuli such as clicks, broadband noise or pure tones. Area S has a sparse distribution of call responsive cells that showed excellent temporal locking, 31% of which selectively responded to a single call. AI responded well to all vocalizations and was much more responsive to vocalizations than the adjacent dorsocaudal core area. Areas VRB, AI and S contained units with the highest levels of mutual information about call stimuli. Area T also responded well to some calls but seems to be specialized for low sound levels. The two dorsal belt areas are comparatively unresponsive to vocalizations and contain little information about the calls. AI projects to areas S, VRB and T, so there may be both rostral and ventral pathways for processing vocalizations in the guinea pig.     

Neuronal selectivity to complex vocalization features emerges in the superficial layers of primary auditory cortex

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.

A study of the neuronal representations elicited in guinea pigs by conspecific calls at different auditory processing stages reveals insights into where call-selective neuronal responses emerge; the transformation from nonselective to call-selective responses occurs in the superficial layers of the primary auditory cortex.     

Reduction of information redundancy in the ascending auditory pathway

Information processing by a sensory system is reflected in the changes in stimulus representation along its successive processing stages. We measured information content and stimulus-induced redundancy in the neural responses to a set of natural sounds in three successive stations of the auditory pathway-inferior colliculus (IC), auditory thalamus (MGB), and primary auditory cortex (A1). Information about stimulus identity was somewhat reduced in single A1 and MGB neurons relative to single IC neurons, when information is measured using spike counts, latency, or temporal spiking patterns. However, most of this difference was due to differences in firing rates. On the other hand, IC neurons were substantially more redundant than A1 and MGB neurons. IC redundancy was largely related to frequency selectivity. Redundancy reduction may be a generic organization principle of neural systems, allowing for easier readout of the identity of complex stimuli in A1 relative to IC.     

Reaction of neurons of the medial geniculate body to acoustic stimulation

Responses of medial geniculate body (MGB) neurons to pure tones and clicks were studied in acute experiments in immobilized cats, preliminary operations being performed under calypsol anaesthesia. MGB units were identified by their reactions to cortical zone AI and brachium of inferior colliculus stimulations. When tonal stimuli were applied relay neurons of pars principalis of MGB usually demonstrated either unimodal tuning curves with narrow frequency band or fragmental ones with several narrow bands. On-response with subsequent inhibition of the background activity or without such an inhibitory period was most frequent type of the reaction (66.6%) of relay MGB neurons to tonal stimulation. The group of relay neurons with the tonic type of reaction (9.1%) was classified for which the duration of tonic response depends on the duration of tonal stimulus. Change of the excitatory reaction to the inhibitory one when the characteristic tone frequency is changed by non-characteristic++ ones is supposed to be a mechanism supplying sharpness of tuning at relay MGB neurons. It is concluded that responses of acoustic cortical neurons to sound stimulation depend to a great extent on the pattern of impulsation that comes from MGB relay units.     

Computational models of temporal processing in the auditory thalamus

Previous work has shown that neurons in the medial geniculate body (MGB) of the echolocating bat, Myotis lucifugus, display response properties that are distinguishable from those of their afferents in the inferior colliculus (IC). Specifically, MGB neurons display phasic temporal discharge patterns, poor entrainment to trains of constant-amplitude sound pulses, and facilitated responses to amplitude-modulated trains of sound pulses (Llano and Feng 1999). In this study we used a modeling approach to examine the relative contributions of different known sources of inhibition on the temporal response properties of auditory thalamocortical neurons. We found that GABA_A-mediated post-excitatory inhibition resulting from coactivation of thalamocortical neurons and local inhibitory interneurons (in a triadic arrangement) is sufficient to reproduce many of the temporal response properties of MGB neurons. Addition of long-duration GABA_B-mediated inhibition gave the thalamocortical neuron temporal response characteristics that more closely resemble those seen in the experimental data. Neither recurrent inhibition from the thalamic reticular nucleus nor post-synaptic nonlinear mechanisms were necessary to reproduce the temporal transformations between the IC and MGB. This work suggests that feed-forward inhibitory circuitry, coupled with slow GABA_B-mediated inhibition, can emulate temporal information processing at the MGB. The transformation taking place in the MGB can be used to extract salient features from complex, time-varying stimuli, such as echoes returning from moving prey. Received: 11 August 1999 / Accepted in revised form: 5 April 2000     

Electrophysiological investigation of conduction of afferent impulses through the medial geniculate body

Extra- and intracellular reactions of 280 neurons of the pars principalis of the medial geniculate body (MGB) and of 408 auditory cortical neurons in area AI to stimulation of the inferior brachium of the midbrain and geniculocortical fibers were studied in cats immobilized with D-tubocurarine. Single electrical stimulation of the inferior brachium was shown to evoke a long and complex neuronal response in MGB in the form of excitation of some and inhibition of other neurons. The initial component of this response lasted 13 msec. Excitation of 72% of neurons participating in the response took place during the first 3 msec after the beginning of stimulation. In the same period 84% of IPSP arose. The inferior brachium was shown to contain a certain number of descending fibers. Some of them are axons of MGB neurons. Many fibers of the inferior brachium reach the auditory cortex without synaptic relay in MGB. Of all cells of MGB excited by stimulation of the inferior brachium monosynaptically, 76% are thalamocortical relay neurons; the rest are interneurons. Of the relay neurons of MGB 90% are excited monosynaptically, the rest by impulses passing through two or three synaptic relays in MGB. During stimulation of the inferior brachium, responses consisting of EPSP-IPSP and primary IPSP are recorded in many neurons of MGB. About 20% of primary IPSP arise monosynaptically, evidently in response to stimulation of inhibitory fibers of the inferior brachium. Most IPSP arise disynaptically, with the participation of an inhibitory interneuron located at the entrance to MGB. Inhibition observed in this case is direct afferent in nature.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 11, No. 6, pp. 515–523, November–December, 1979.     

Signal components, acoustic preference functions and sexual selection in a cricket

In many sexually reproducing organisms, females choose mates based on multiple male traits. This study examined how two temporal components of the male mating call – chirp rate and chirp duration – affect female mating preference in five populations of a widely distributed North American cricket, Allonemobius socius (Orthoptera, Gryllidae). Chirp rate and chirp duration of the A. socius mating call were varied independently, and the responses of virgin females to these experimentally manipulated calls were repeatedly measured using a sequential single-stimulus design. Significant among- and within-population variation in chirp-duration preferences of females were found. Contrary to many previous studies, call chirp rate had no effect on female phonotaxis. Also there was no evidence of an interaction between chirp rate and chirp duration on female response to male mating calls. Moreover, female responsiveness to average and above-average chirp duration appeared to decline with female (adult) age. Overall, these results suggest evolved differences among populations in chirp-duration preferences, and that selection can act within populations on female chirp-duration preference.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 461–472.     

Variation in and Meaning of Alarm Calls in a Social Desert Rodent Rhombomys opimus

The great gerbil (Rhombomys opimus), a social rodent that lives in family groups, emits three different alarm vocalizations in the presence of predators: a rhythmic call; a faster more intense call; and a single whistle. We tested the hypothesis that the alarm calls communicate risk of predation. We quantified the relationship between predator distance and type of alarm call via human approaches to gerbils. We also tested responses of focal adults in family groups to playback broadcasts of the different calls and controls of bird song and tape noise. Results showed that alarm calls were related to distance from a predator. Gerbils gave the rhythmic call when the predator was farthest away, the more intense call as the predator moved closer; and a short whistle when startled by a close approach of the predator. Gerbils stopped feeding and stood vigilant in a frozen alert posture in response to playbacks of all three alarm calls. They decreased non‐vigilant behavior to the alarm vocalizations more than to the controls and decreased non‐vigilant behavior significantly more in response to the intense alarm and whistle compared with the rhythmic alarm. We conclude that one function of gerbil alarm calls is to communicate response urgency to family members. The rhythmic alarm communicates danger at a distance, whereas the intense alarm and whistle signal the close approach of a predator.     

Sequential phases of cortical specification involve Neurogenin-dependent and -independent pathways

Neocortical projection neurons, which segregate into six cortical layers according to their birthdate, have diverse morphologies, axonal projections and molecular profiles, yet they share a common cortical regional identity and glutamatergic neurotransmission phenotype. Here we demonstrate that distinct genetic programs operate at different stages of corticogenesis to specify the properties shared by all neocortical neurons. Ngn1 and Ngn2 are required to specify the cortical (regional), glutamatergic (neurotransmitter) and laminar (temporal) characters of early-born (lower-layer) neurons, while simultaneously repressing an alternative subcortical, GABAergic neuronal phenotype. Subsequently, later-born (upper-layer) cortical neurons are specified in an Ngn-independent manner, requiring instead the synergistic activities of Pax6 and Tlx, which also control a binary choice between cortical/glutamatergic and subcortical/GABAergic fates. Our study thus reveals an unanticipated heterogeneity in the genetic mechanisms specifying the identity of neocortical projection neurons.     

Acoustically induced call modification in the white-lipped frog,Leptodactylus albilabris

The vocalization behaviour of Leptodactylus albilabris was investigated using field playback experiments. To assess the response of males to pre-recorded natural ‘chirp’ (advertisement call) and natural ‘chuckle” (aggressive call) stimuli of gradually increasing broadcast intensity, three parameters (intensity, dominant frequency and repetition rate) of the chirp call were analysed. Of the males tested, 69% showed a significant increase in chirp intensity with increased levels of both stimulus types. In response to playback of the chirp stimulus, males actively modified the dominant frequency of their chirp calls over a mean range of 91·42 Hz, and in one case as much as 400 Hz. Moreover, 12 of 17 males shifted the frequency of their call towards the dominant frequency of the chirp stimulus (2175 Hz) by either increasing or decreasing the dominant frequency of their chirp calls. In response to the natural chuckle stimulus, 83% of the males showed either a decrease or no significant change in the dominant frequency of their chirps. All eight males for which both the chirp frequency and intensity were analysed and that showed an increase in chirp intensity also showed a concomitant increase in chirp dominant frequency. These results are the first to document quantitatively the plasticity of advertisement call intensity and dominant frequency in an anuran. The possible effects of advertisement call modification on male mating success in L. albilabris is discussed.     

Age Differences in the Response of California Ground Squirrels (Spermophilus beecheyi) to Conspecific Alarm Calls

Juvenile California ground squirrel responses to adult alarm calls and juvenile alarm calling may be modified during development to achieve adult form. Adult conspecific chatter and whistle alarm calls were played back to juvenile and adult ground squirrels at an agricultural field site. In response to chatter playbacks, adults spent more time visually orienting to the environment and less time out of view and in covered habitats than juveniles; the converse was true in response to whistle playbacks. To test the evocativeness of juvenile calling, a subset of adult subjects received juvenile chatter and whistle playbacks. Adults spent less time out of view to juvenile call types than to adult calls, and showed more similar responses to juvenile chatters and whistles than to adult chatters and whistles. Age differences in the ground squirrel's alarm call system may reflect adjustments to changing risks during development.     

Thalamic activation modulates the responses of neurons in rat primary auditory cortex: an in vivo intracellular recording study

Auditory cortical plasticity can be induced through various approaches. The medial geniculate body (MGB) of the auditory thalamus gates the ascending auditory inputs to the cortex. The thalamocortical system has been proposed to play a critical role in the responses of the auditory cortex (AC). In the present study, we investigated the cellular mechanism of the cortical activity, adopting an in vivo intracellular recording technique, recording from the primary auditory cortex (AI) while presenting an acoustic stimulus to the rat and electrically stimulating its MGB. We found that low-frequency stimuli enhanced the amplitudes of sound-evoked excitatory postsynaptic potentials (EPSPs) in AI neurons, whereas high-frequency stimuli depressed these auditory responses. The degree of this modulation depended on the intensities of the train stimuli as well as the intervals between the electrical stimulations and their paired sound stimulations. These findings may have implications regarding the basic mechanisms of MGB activation of auditory cortical plasticity and cortical signal processing.     

Geographic variation in female preference functions and male songs of the field cricket Teleogryllus oceanicus

Male crickets (Teleogryllus oceanicus) produce a complex call consisting of two elements, the long chirp (three to eight sound pulses) followed by a series of short chirps (each with two sound pulses). There is significant geographic variation in the temporal structure of calls, and the long chirp is selected against by acoustically orienting parasitoids in some populations. Here we examine geographic variation in female preference functions for the amount of long chirp. In general, females prefer calls with greater proportions of long chirp, although the strength and nature of selection varied across populations. Variation in preference functions did not match variation in call structure. There was a mismatch between the proportion of long chirp produced by males in a population and the proportion of long chirp preferred by females. The convergent preferences of predators and females are likely to maintain genetic variation in song traits in parasitized populations. The apparent mismatch between preference and trait is discussed in relation to theoretical models of preference evolution.     

Mean field model of acetylcholine mediated dynamics in the cerebral cortex

A recent continuum model of the large scale electrical activity of the cerebral cortex is generalized to include cholinergic modulation. In this model, dynamic modulation of synaptic strength acts over the time scales of nicotinic and muscarinic receptor action. The cortical model is analyzed to determine the effect of acetylcholine (ACh) on its steady states, linear stability, spectrum, and temporal responses to changes in subcortical input. ACh increases the firing rate in steady states of the system. Changing ACh concentration does not introduce oscillatory behavior into the system, but increases the overall spectral power. Model responses to pulses in subcortical input are affected by the tonic level of ACh concentration, with higher levels of ACh increasing the magnitude firing rate response of excitatory cortical neurons to pulses of subcortical input. Numerical simulations are used to explore the temporal dynamics of the model in response to changes in ACh concentration. Evidence is seen of a transition from a state in which intracortical inputs are emphasized to a state where thalamic afferents have enhanced influence. Perturbations in ACh concentration cause changes in the firing rate of cortical neurons, with rapid responses due to fast acting facilitatory effects of nicotinic receptors on subcortical afferents, and slower responses due to muscarinic suppression of intracortical connections. Together, these numerical simulations demonstrate that the actions of ACh could be a significant factor modulating early components of evoked response potentials.     

Stimulus-specific adaptation in the auditory thalamus of the anesthetized rat

The specific adaptation of neuronal responses to a repeated stimulus (Stimulus-specific adaptation, SSA), which does not fully generalize to other stimuli, provides a mechanism for emphasizing rare and potentially interesting sensory events. Previous studies have demonstrated that neurons in the auditory cortex and inferior colliculus show SSA. However, the contribution of the medial geniculate body (MGB) and its main subdivisions to SSA and detection of rare sounds remains poorly characterized. We recorded from single neurons in the MGB of anaesthetized rats while presenting a sequence composed of a rare tone presented in the context of a common tone (oddball sequences). We demonstrate that a significant percentage of neurons in MGB adapt in a stimulus-specific manner. Neurons in the medial and dorsal subdivisions showed the strongest SSA, linking this property to the non-lemniscal pathway. Some neurons in the non-lemniscal regions showed strong SSA even under extreme testing conditions (e.g., a frequency interval of 0.14 octaves combined with a stimulus onset asynchrony of 2000 ms). Some of these neurons were able to discriminate between two very close frequencies (frequency interval of 0.057 octaves), revealing evidence of hyperacuity in neurons at a subcortical level. Thus, SSA is expressed strongly in the rat auditory thalamus and contribute significantly to auditory change detection.     

The auditory cortex

The division of the auditory cortex into various fields, functional aspects of these fields, and neuronal coding in the primary auditory cortical field (AI) are reviewed with stress on features that may be common to mammals. On the basis of 14 topographies and clustered distributions of neuronal response characteristics in the primary auditory cortical field, a hypothesis is developed of how a certain complex acoustic pattern may be encoded in an equivalent spatial activity pattern in AI, generated by time-coordinated firing of groups of neurons. The auditory cortex, demonstrated specifically for AI, appears to perform sound analysis by synthesis, i.e. by combining spatially distributed coincident or time-coordinated neuronal responses. The dynamics of sounds and the plasticity of cortical responses are considered as a topic for research. Accepted: 25 July 1997     

Bilateral collicular interaction: modulation of auditory signal processing in amplitude domain

In the ascending auditory pathway, the inferior colliculus (IC) receives and integrates excitatory and inhibitory inputs from many lower auditory nuclei, intrinsic projections within the IC, contralateral IC through the commissure of the IC and from the auditory cortex. All these connections make the IC a major center for subcortical temporal and spectral integration of auditory information. In this study, we examine bilateral collicular interaction in modulating amplitude-domain signal processing using electrophysiological recording, acoustic and focal electrical stimulation. Focal electrical stimulation of one (ipsilateral) IC produces widespread inhibition (61.6%) and focused facilitation (9.1%) of responses of neurons in the other (contralateral) IC, while 29.3% of the neurons were not affected. Bilateral collicular interaction produces a decrease in the response magnitude and an increase in the response latency of inhibited IC neurons but produces opposite effects on the response of facilitated IC neurons. These two groups of neurons are not separately located and are tonotopically organized within the IC. The modulation effect is most effective at low sound level and is dependent upon the interval between the acoustic and electric stimuli. The focal electrical stimulation of the ipsilateral IC compresses or expands the rate-level functions of contralateral IC neurons. The focal electrical stimulation also produces a shift in the minimum threshold and dynamic range of contralateral IC neurons for as long as 150 minutes. The degree of bilateral collicular interaction is dependent upon the difference in the best frequency between the electrically stimulated IC neurons and modulated IC neurons. These data suggest that bilateral collicular interaction mainly changes the ratio between excitation and inhibition during signal processing so as to sharpen the amplitude sensitivity of IC neurons. Bilateral interaction may be also involved in acoustic-experience-dependent plasticity in the IC. Three possible neural pathways underlying the bilateral collicular interaction are discussed.     

Temporal selectivity for complex signals by single neurons in the torus semicircularis of Pleurodema thaul (Amphibia: Leptodactylidae)

Responses of auditory neurons in the torus semicircularis (TS) of Pleurodema thaul, a leptodactylid from Chile, to synthetic stimuli having diverse temporal patterns and to digitized advertisement calls of P. thaul and three sympatric species, were recorded to investigate their temporal response selectivities. The advertisement call of this species consists of a long sequence of sound pulses (a pulse-amplitude-modulated, or PAM, signal) having a dominant frequency of about 2000 Hz. Each of the sound pulses contains intra-pulse sinusoidal-amplitude-modulations (SAMs). Synthetic stimuli consisted of six series in which the following acoustic parameters were systematically modified, one at a time: PAM rate, pulse duration, number of pulses, and intra-pulse SAM rate. The carrier frequency of these stimuli was set at the characteristic frequency (CF) of the isolated units (n = 47). Response patterns of TS units to synthetic call variants reveal different degrees of selectivities for each of the temporal variables, with populations of neurons responding maximally to specific values found in the advertisement call of this species. These selectivities are mainly shaped by neuronal responsiveness to the overall sound energy of the stimulus and by the inability of neurons to discharge to short inter-pulse gaps. Accepted: 30 October 1996