To identify sounds as novel, there must be some neural representation of commonly occurring sounds. Stimulus-specific adaptation (SSA) is a reduction in neural response to a repeated sound. Previous studies using an oddball stimulus paradigm have shown that SSA occurs at the cortex, but this study demonstrates that neurons in the inferior colliculus (IC) also show strong SSA using this paradigm. The majority (66%) of IC neurons showed some degree of SSA. Approximately 18% of neurons showed near-complete SSA. Neurons with SSA were found throughout the IC. Responses of IC neurons were reduced mainly during the onset component of the response, and latency was shorter in response to the oddball stimulus than to the standard. Neurons with near-complete SSA were broadly tuned to frequency, suggesting a high degree of convergence. Thus, some of the mechanisms that may underlie novelty detection and behavioral habituation to common sounds are already well developed at the midbrain.

Duration is a biologically important feature of sound. Some neurons in the inferior colliculus of the big brown bat, Eptesicus fuscus, are tuned to sound duration, but it is unclear at what level the tuning originates or what neural mechanisms are responsible for it. The application of antagonists of the inhibitory neurotransmitters gamma-aminobutyric acid or glycine to neurons in the inferior colliculus eliminated duration tuning. Whole-cell patch-clamp recordings of synaptic currents suggested that inhibition produces a temporal frame within which excitation can occur. A model is proposed in which duration tuning arises when an early, sustained inhibitory input interacts with a delayed, transient excitatory input.

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 inferior colliculus (IC) is the first place in the central auditory pathway where duration-selective neurons are found. Previous neuropharmacological and electrophysiological studies have shown that they are created there and have led to a conceptual model in which excitatory and inhibitory inputs are offset in time so that the cell fires only when sound duration is such that onset-and offsetevoked excitation coincide; the response is suppressed by inhibition at other durations. We tested predictions from the model using paired tone stimulation and extracellular recording in the IC of the big brown bat, Eptesicus fuscus. Responses to a best duration (BD) tone were used as a probe to examine the strength and time course of inhibition activated by a nonexcitatory (NE) tone of the same frequency but differing in duration. As the relative time between the BD and NE tones was varied, the activity evoked by the BD tone was affected in ways comparable with backward, simultaneous, and forward masking. Responses to the BD tone were completely suppressed at short interstimulus intervals when the BD tone preceded the NE tone. Suppression was also seen when the stimuli temporally overlapped and summed and at intervals when the BD tone followed the NE tone. The results show that duration-selective neurons receive an onsetevoked, inhibitory input that precedes their excitatory input. The period of leading inhibition was correlated with BD and first spike latency. The results suggest how inhibition in the CNS could explain temporal masking phenomena, including backward masking.

In echolocating bats, three cell groups in the lateral lemniscus are conspicuous for their large size and high degree of differentiation. These cell groups are the intermediate nucleus (INLL), columnar nucleus (VNLLc), and multipolar cell area (VNLLm). All receive projections from the contralateral cochlear nucleus. Previous anatomical studies suggest the hypothesis that these nuclei are important for analyzing the temporal structure of sound. To investigate this possibility, we recorded responses of single units in the INLL, VNLLc, and VNLLm of Eptesicus fuscus. The results show that each cytoarchitectural division contains a complete tonotopic representation. Certain response properties are common to all three nuclei. First, virtually all units are monaural. Second, all are broadly tuned to frequency; their average Q10dB value of 9.1 is considerably lower than values measured in the inferior colliculus of Eptesicus. Third, most units have little or no spontaneous activity. Fourth, all have short integration times, responding robustly to stimuli less than 5 msec in duration. The broad tuning, lack of spontaneous activity, and short integration time all make these neurons well suited for the accurate encoding of temporal information. Although there are many similarities, there are also important differences among nuclei. The clearest evidence of specialization is in VNLLc. Neurons here are more broadly tuned than those in INLL or VNLLm, have no spontaneous activity, and always respond with one spike per stimulus. The latency of the spike is precisely locked to the stimulus onset, with variability from trial to trial as low as 0.03 msec. In addition, the latency remains constant over large variations in frequency or intensity. In INLL and VNLLm, response patterns are about equally distributed between tonic, chopping, and phasic; there are no single-spike constant-latency responses of the type seen in VNLLc, although some choppers and pausers do respond with constant first-spike latency. The results indicate that VNLLc is specialized to encode very precisely the onset of sound; the other nuclei may encode ongoing properties of a sound.

Novel stimuli in all sensory modalities are highly effective in attracting and focusing attention. Stimulus-specific adaptation (SSA) and brain activity evoked by novel stimuli have been studied using population measures such as imaging and event-related potentials, but there have been few studies at the single-neuron level. In this study we compare SSA across different populations of neurons in the inferior colliculus (IC) of the rat and show that a subclass of neurons with rapid and pronounced SSA respond selectively to novel sounds. These neurons, located in the dorsal and external cortex of the IC, fail to respond to multiple repetitions of a sound but briefly recover their excitability when some stimulus parameter is changed. The finding of neurons that respond selectively to novel stimuli in the mammalian auditory midbrain suggests that they may contribute to a rapid subcortical pathway for directing attention and/or orienting responses to novel sounds.

BackgroundSocial alarm calls alert animals to potential danger and thereby promote group survival. Adult laboratory rats in distress emit 22-kHz ultrasonic vocalization (USV) calls, but the question of whether these USV calls directly elicit defensive behavior in conspecifics is unresolved.Methodology/Principal FindingsThe present study investigated, in pair-housed male rats, whether and how the conditioned fear-induced 22-kHz USVs emitted by the ‘sender’ animal affect the behavior of its partner, the ‘receiver’ animal, when both are placed together in a novel chamber. The sender rats’ conditioned fear responses evoked significant freezing (an overt evidence of fear) in receiver rats that had previously experienced an aversive event but not in naïve receiver rats. Permanent lesions and reversible inactivations of the medial geniculate nucleus (MGN) of the thalamus effectively blocked the receivers’ freeezing response to the senders' conditioned fear responses, and this occurred in absence of lesions/inactivations impeding the receiver animals' ability to freeze and emit 22-kHz USVs to the aversive event per se.Conclusions/SignificanceThese results—that prior experience of fear and intact auditory system are required for receiver rats to respond to their conspecifics' conditioned fear responses—indicate that the 22-kHz USV is the main factor for social transmission of fear and that learning plays a crucial role in the development of social signaling of danger by USVs.

Neural tuning to different sound durations may be a useful filter for identification of certain sounds, especially those that are biologically important. The auditory midbrains of mammals and amphibians contain neurons that appear to be tuned to sound duration. In amphibians, neurons are tuned to durations of sound that are biologically important. The purpose of this study was to characterize responses of neurons in the inferior colliculus (IC) of the big brown bat, Eptesicus fuscus, to sounds of different durations. Our aims were to determine what percent of neurons are duration tuned and how best durations are correlated to durations of echolocation calls, and to examine response properties that may be relevant to the mechanism for duration tuning, such as latency and temporal firing pattern; we also examined frequency tuning and rate-level functions. We recorded from 136 single units in the central nucleus of the IC of unanesthetized bats. The stimuli were pure tones, frequency-modulated sweeps, and broadband noise. The criterion for duration tuning was an increase in spike count of > or = 50% at some durations compared with others. Of the total units sampled, 36% were tuned to stimulus duration. All of these units were located in the caudal half of the IC. Best duration for most units ranged from < 1 to 10 ms, but a few had best durations up to > or = 20 ms. This range is similar to the range of durations of echolocation calls used by Eptesicus. All duration-tuned neurons responded transiently. The minimum latency was always longer than the best duration. Duration-tuned units have best durations and best frequencies that match the temporal structure and frequency range of the echolocation calls. Thus the results raise the hypothesis that neurons in the IC of Eptesicus, and probably the auditory midbrain of other vertebrates, are tuned to biologically important sound durations. We suggest a model for duration tuning consisting of three components: 1) inhibitory input that is correlated with the onset of the stimulus and is sustained for the stimulus duration; 2) transient excitation that is correlated with the offset of the stimulus; and 3) transient excitation that is correlated with the onset of the stimulus but is delayed in time relative to the onset of inhibition. For the neuron to fire, the two excitatory events must coincide in time; noncoincident excitatory events are not sufficient.