Behavioral Neuroscience publications

This study examines patterns of neural activity in response to single biphasic electrical pulses, presented alone or following a forward masking pulse train, delivered by a cochlear implant. Recordings were made along the tonotopic axis of the central nucleus of the inferior colliculus (ICC) in ketamine/xylazine anesthetized guinea pigs. The partial tripolar electrode configuration was used, which provided a systematic way to vary the tonotopic extent of ICC activation between monopolar (broad) and tripolar (narrow) extremes while maintaining the same peak of activation. The forward masking paradigm consisted of a 200 ms masker pulse train (1017 pulses per second) followed 10 ms later by a single-pulse probe stimulus; the current fraction of the probe was set to 0 (monopolar), 1 (tripolar), or 0.5 (hybrid), and the fraction of the masker was fixed at 0.5. Forward masking tuning profiles were derived from the amount of masking current required to just suppress the activity produced by a fixed-level probe. These profiles were sharper for more focused probe configurations, approximating the pattern of neural activity elicited by single (non-masked) pulses. The result helps to bridge the gap between previous findings in animals and recent psychophysical data.

The efficient-coding hypothesis asserts that neural and perceptual sensitivity evolved to faithfully represent biologically relevant sensory signals. Here we characterized the spectrotemporal modulation statistics of several natural sound ensembles and examined how neurons encode these statistics in the central nucleus of the inferior colliculus (CNIC) of cats. We report that modulation-tuning in the CNIC is matched to equalize the modulation power of natural sounds. Specifically, natural sounds exhibited a tradeoff between spectral and temporal modulations, which manifests as 1/ f modulation power spectrum (MPS). Neural tuning was highly overlapped with the natural sound MPS and neurons approximated proportional resolution filters where modulation bandwidths scaled with characteristic modulation frequencies, a behavior previously described in human psychoacoustics. We demonstrate that this neural scaling opposes the 1/ f scaling of natural sounds and enhances the natural sound representation by equalizing their MPS. Modulation tuning in the CNIC may thus have evolved to represent natural sound modulations in a manner consistent with efficiency principles and the resulting characteristics likely underlie perceptual resolution.

Recognition of acoustic signals may be impeded by two factors: extrinsic noise, which degrades sounds before they arrive at the receiver's ears, and intrinsic neuronal noise, which reveals itself in the trial-to-trial variability of the responses to identical sounds. Here we analyzed how these two noise sources affect the recognition of acoustic signals from potential mates in grasshoppers. By progressively corrupting the envelope of a female song, we determined the critical degradation level at which males failed to recognize a courtship call in behavioral experiments. Using the same stimuli, we recorded intracellularly from auditory neurons at three different processing levels, and quantified the corresponding changes in spike train patterns by a spike train metric, which assigns a distance between spike trains. Unexpectedly, for most neurons, intrinsic variability accounted for the main part of the metric distance between spike trains, even at the strongest degradation levels. At consecutive levels of processing, intrinsic variability increased, while the sensitivity to external noise decreased. We followed two approaches to determine critical degradation levels from spike train dissimilarities, and compared the results with the limits of signal recognition measured in behaving animals.

The center-out task is a standard paradigm often used to study the neural control of reaching movements in human and non-human primates. However, there are several disadvantages to the use of monkeys, notably costs, infrastructural requirements, and ethical considerations. Here we describe a similar task designed to examine forelimb movements in rats. Rats were trained to grasp a joystick with their forepaw and use it to control the movements of a sipper tube in two dimensions. The rats learned to move the joystick in four directions with at least 70% accuracy after about 45 days of training. In addition, rats were able to learn a reversed mapping between joystick and sipper tube movement. This is a more complicated behavior than has been previously demonstrated for rats, and it could allow more motor behavior studies to be conducted in rodents instead of monkeys. We currently are using this behavior to decode the rats' forelimb movements from their brain signals.

Belgian Waterslager (BW) canaries have an inherited hearing loss due to missing and abnormal hair cells, but it is unclear whether the loss is congenital or developmental. We used auditory brainstem responses and scanning electron microscopy to describe the development of auditory sensitivity and hair cell abnormalities in BW and non-BW canaries. In both strains, adult ABR thresholds were higher than behavioral thresholds, but BW canaries exhibited higher thresholds than non-BW canaries across all frequencies. Immediately post-hatch, ABR thresholds and hair cell numbers were similar in both strains. Two weeks later, thresholds were significantly higher in BW canaries, and hair cell number progressively decreased as the birds aged. These data show that in BW canaries: the peripheral auditory system is functionally similar to non-BW canary from hatch to 2 weeks, ABR thresholds improve during this developmental period, actually becoming better than those of adults, but then worsen as the bird continues to age. Hair cell number and appearance is similar to non-BW canaries at hatch but progressively declines after 30 days of age. These data show that the hearing loss characteristic of BW canaries is, at least in part, developmental and is established by the time song learning begins.

The pitch of the missing fundamental (F0) is one of the principal psychological attributes of human pitch perception. Behavioral responses to harmonic tone complexes having missing F0s were measured in chinchillas using operant conditioning and stimulus generalization. Animals were trained to discriminate between tone complexes having a 500-Hz F0 and a 125-Hz F0. When animals were tested with tone complexes having the same F0s, but where the F0s were missing, responses were similar to those obtained when the F0s were present, suggesting that missing F0 sounds were perceptually equivalent to F0 present sounds. Behavioral responses to F0 present and missing F0 stimuli were similar in the presence of low-pass masking noise, suggesting that the perception was not due to the reinsertion of the F0 through cochlear nonlinearities. Gradients in behavioral responses were observed when the F0s of test complexes were systematically varied, suggesting the existence of a psychological dimension related to F0. Behavioral responses were related to the F0 rather than to spectral differences among test stimuli when the F0 and spectrum were varied independently. The results indicate that chinchillas possess a pitch-like perception of the missing F0 that is unlikely to arise from cochlear distortion products.

Many fishes rely on their auditory skills to interpret crucial information about predators and prey, and to communicate intraspecifically. Few studies, however, have examined how complex natural sounds are perceived in fishes. We investigated the representation of conspecific mating and agonistic calls in the auditory system of the Lusitanian toadfish Halobatrachus didactylus , and analysed auditory responses to heterospecific signals from ecologically relevant species: a sympatric vocal fish (meagre Argyrosomus regius ) and a potential predator (dolphin Tursiops truncatus ). Using auditory evoked potential (AEP) recordings, we showed that both sexes can resolve fine features of conspecific calls. The toadfish auditory system was most sensitive to frequencies well represented in the conspecific vocalizations (namely the mating boatwhistle), and revealed a fine representation of duration and pulsed structure of agonistic and mating calls. Stimuli and corresponding AEP amplitudes were highly correlated, indicating an accurate encoding of amplitude modulation. Moreover, Lusitanian toadfish were able to detect T. truncatus foraging sounds and A. regius calls, although at higher amplitudes. We provide strong evidence that the auditory system of a vocal fish, lacking accessory hearing structures, is capable of resolving fine features of complex vocalizations that are probably important for intraspecific communication and other relevant stimuli from the auditory scene.

The perceptual salience and visibility of image elements is influenced by other elements in their vicinity. The perceptual effect of image elements on an adjacent target element depends on their relative orientation. Collinear flanking elements usually improve sensitivity for the target element, whereas orthogonal elements have a weaker effect. It is believed that the collinear flankers exert these effects through lateral interactions between neurons in the primary visual cortex (area V1), but the precise mechanisms underlying these contextual interactions remain unknown. Here, we directly examined this question by recording the effects of flankers on the responses of V1 neurons at parafoveal representations while monkeys performed a fixation task or a contrast detection task. We found, unexpectedly, that collinear flankers reduce the monkeys' perceptual sensitivity for a central target element. This behavioral effect was explained by a flanker-induced increase in the activity of V1 neurons in the absence of the central target stimulus, which reduced the amplitude of the target response. Our results indicate that the dominant effect of collinear flankers in parafoveal vision is suppression and suggest that these suppressive effects are caused by a decrease in the dynamic range of neurons coding the central target.

Segregation of concurrent sounds in complex acoustic environments is a fundamental feature of auditory scene analysis. A powerful cue used by the auditory system to segregate concurrent sounds, such as speakers' voices at a cocktail party, is inharmonicity. This can be demonstrated when a component of a harmonic complex tone is perceived as a separate tone “popping out” from the complex as a whole when it is sufficiently mistuned from its harmonic value. The neural bases of perceptual “pop out” of mistuned harmonics are unclear. We recorded multiunit activity from primary auditory cortex (A1) of behaving monkeys elicited by harmonic complex tones that were either “in tune” or that contained a mistuned third harmonic set at the best frequency of the neural populations. Responses to mistuned sounds were enhanced relative to responses to “in-tune” sounds, thus correlating with the enhanced perceptual salience of the mistuned component. Consistent with human psychophysics of “pop out,” response enhancements increased with the degree of mistuning, were maximal for neural populations tuned to the frequency of the mistuned component, and were not observed under comparable stimulus conditions that do not elicit perceptual “pop out.” Mistuning was also associated with changes in neuronal temporal response patterns phase locked to “beats” in the stimuli. Intracortical auditory evoked potentials paralleled noninvasive neurophysiological correlates of perceptual “pop out” in humans, further augmenting the translational relevance of the results. Findings suggest two complementary neural mechanisms for “pop out,” based on the detection of local differences in activation level or coherence of temporal response patterns across A1.

The intensity of a noise-induced startle response can be reduced by the presentation of an otherwise neutral stimulus immediately before the noise ("prepulse inhibition" or PPI). We used a form of PPI to study the effects of damage to auditory cortex on the discrimination of speech sounds by rats. Subjects underwent control surgery or treatment of the auditory cortex with the vasoconstrictor endothelin-1. This treatment caused damage concentrated in primary auditory cortex (A1). Both before and after lesions, subjects were tested on 5 tasks, most presenting a pair of human speech sounds (consonant-vowel syllables) so that the capacity for discrimination would be evident in the extent of PPI. Group comparisons failed to reveal any consistent lesion effect. At the same time, the analysis of individual differences in performance by multiple regression suggests that some of the temporal processing required to discriminate speech sounds is concentrated anteroventrally in the right A1. These results also confirm that PPI can be adapted to studies of the brain mechanisms involved in the processing of speech and other complex sounds.

Songbirds, which, like humans, learn complex vocalizations, provide an excellent model for the study of acoustic pattern recognition. Here we examined the role of three basic acoustic parameters in an ethologically relevant categorization task. Female zebra finches were first trained to classify songs as belonging to one of two males and then asked whether they could generalize this knowledge to songs systematically altered with respect to frequency, timing, or intensity. Birds' performance on song categorization fell off rapidly when songs were altered in frequency or intensity, but they generalized well to songs that were changed in duration by >25%. Birds were not deaf to timing changes, however; they detected these tempo alterations when asked to discriminate between the same song played back at two different speeds. In addition, when birds were retrained with songs at many intensities, they could correctly categorize songs over a wide range of volumes. Thus although they can detect all these cues, birds attend less to tempo than to frequency or intensity cues during song categorization. These results are unexpected for several reasons: zebra finches normally encounter a wide range of song volumes but most failed to generalize across volumes in this task; males produce only slight variations in tempo, but females generalized widely over changes in song duration; and all three acoustic parameters are critical for auditory neurons. Thus behavioral data place surprising constraints on the relationship between previous experience, behavioral task, neural responses, and perception. We discuss implications for models of auditory pattern recognition.

Adult rats were trained to detect the occurrence of a two-element sound sequence in a background of nine other nontarget sound pairs. Training resulted in a modest, enduring, static expansion of the cortical areas of representation of both target stimulus sounds. More importantly, once the initial stimulus A in the target A-B sequence was presented, the cortical “map” changed dynamically, specifically to exaggerate further the representation of the “anticipated” stimulus B. If B occurred, it was represented over a larger cortical area by more strongly excited, more coordinated, and more selectively responding neurons. This biasing peaked at the expected time of B onset with respect to A onset. No dynamic biasing of responses was recorded for any sound presented in a nontarget pair. Responses to nontarget frequencies flanking the representation of B were reduced in area and in response strength only after the presentation of A at the expected time of B onset. This study shows that cortical areas are not representationally static but, to the contrary, can be biased moment by moment in time as a function of behavioral context.

Although lizards have highly sensitive ears, it is difficult to condition them to sound, making standard psychophysical assays of hearing sensitivity impractical. This paper describes non-invasive measurements of the auditory brainstem response (ABR) in both Tokay geckos (Gekko gecko; nocturnal animals, known for their loud vocalizations) and the green anole (Anolis carolinensis, diurnal, non-vocal animals). Hearing sensitivity was measured in 5 geckos and 7 anoles. The lizards were sedated with isoflurane, and ABRs were measured at levels of 1 and 3% isoflurane. The typical ABR waveform in response to click stimulation showed one prominent and several smaller peaks occurring within 10 ms of the stimulus onset. ABRs to brief tone bursts revealed that geckos and anoles were most sensitive between 1.6–2 kHz and had similar hearing sensitivity up to about 5 kHz (thresholds typically 20–50 dB SPL). Above 5 kHz, however, anoles were more than 20 dB more sensitive than geckos and showed a wider range of sensitivity (1–7 kHz). Generally, thresholds from ABR audiograms were comparable to those of small birds. Best hearing sensitivity, however, extended over a larger frequency range in lizards than in most bird species.

The auditory system has two parallel streams in the brain that have been implicated in auditory fear learning. The lemniscal stream has selective neurons that are tonotopically organized and is thought to be important for sound discrimination. The nonlemniscal stream has less selective neurons, which are not tonotopically organized, and is thought to be important for multimodal processing and for several forms of learning. Therefore, it has been hypothesized that the lemniscal, but not the nonlemniscal, pathway supports discriminative fear to auditory cues. To test this hypothesis we assessed the effect of electrolytic lesions to the ventral, or medial, division of the medial geniculate nucleus (MGv or MGm, which correspond, respectively, to the lemniscal and the nonlemniscal auditory pathway to amygdala) on the acquisition, expression and extinction of fear responses in discriminative auditory fear conditioning, where one tone is followed by shock (conditioned stimulus, CS(+)), and another is not (CS(-)). Here we show that with single-trial conditioning control, MGv- and MGm-lesioned male rats acquire nondiscriminative fear of both the CS(+) and the CS(-). However, after multiple-trial conditioning, control rats discriminate between the CS(+) and CS(-), whereas MGv- and MGm-lesioned do not. Furthermore, post-training lesions of MGm, but not MGv, lead to impaired expression of discriminative fear. Finally, MGm-lesioned rats display high levels of freezing to both the CS(+) and CS(-) even after an extinction session to the CS(+). In summary, our findings suggest that the lemniscal pathway is important for discriminative learning, whereas the nonlemniscal is important for negatively regulating fear responses.

Psychophysical studies show a slower response to changes in the specifically binaural input than to changes in the monaural input (binaural sluggishness). However, there is disagreement about the time course. Tracking changes in a target yields fast time constants, while detecting a constant target against a varying background yields the slowest. Changes in the binaural properties of a target are tracked up to high rates by cells in the midbrain. Indeed cells respond rapidly to a step change and then the firing rate slowly adapts. These experiments, though, are analogues of psychophysical experiments that give the faster time constants. Sluggishness should be more apparent physiologically in a binaural masking paradigm, detecting a short tone in a noise masker with a step change in masker correlation: the small change in firing rate due to the signal must be detected against the adapting firing rate change caused by the step change in the masker. However, in 40 inferior colliculus cells in the anesthetized guinea pig, in a direct analogue of the psychophysical masking paradigm, measuring thresholds for short tones across a transition in a binaural masker (e.g., from N0S0 to NπS0) provided little evidence of sluggishness within individual cells despite masking level differences in these cells comparable with previous data. Previous studies of physiological correlates of binaural masking level difference suggested that different psychophysical thresholds arise from different populations of cells. This suggests the hypothesis that sluggishness may result from a change in focus between the different populations of cells signaling threshold in different binaural configurations rather than within the intrinsic properties of the cells themselves.

Background: Salicylate and quinine have been shown to reliably induce short-term tinnitus when administered at high doses. The present study compared salicylate and quinine-induced tinnitus in rats using the gap prepulse inhibition of acoustic startle (GPIAS). Methods: Twenty-four rats were divided into 2 groups; the first group (n = 12) was injected with salicylate (300 mg kg d), whereas the second (n = 12) was treated with quinine orally at a dose of 200 mg kg d. Animals were treated daily for 4 consecutive days. All rats were tested for tinnitus and hearing loss before and 2, 24, 48, 72, and 96 hours after the first drug administration. Tinnitus was assessed using GPIAS; hearing function was measured with distortion product otoacoustic emissions (DPOAEs) and auditory brainstem response. Results: Salicylate treatment induced transient tinnitus with a pitch near 16 kHz starting 2 hours posttreatment, persisting over the 4-day treatment period and disappearing 24 hours later. Animals in the quinine group showed GPIAS changes at a higher pitch (20 kHz); however, changes were more variable among animals, and the mean data were not statistically significant. Hearing function varied across treatments. In the salicylate group, high-level DPOAEs were slightly affected; most changes occurred 2 hours posttreatment. Low-level DPOAEs were affected at all frequencies with a progressive dose-dependent effect. In the quinine group, only high-level DPOAEs were affected, mainly at 16 kHz. Conclusion: The present study highlights the similarities and differences in the frequency and the time course of tinnitus and hypoacusis induced by salicylate and quinine. Transient tinnitus was reliably induced pharmacologically with salicylate, whereas hearing loss remained subclinical with only minor changes in DPOAEs.

In humans, auditory perception reaches maturity over a broad age range, extending through adolescence. Despite this slow maturation, children are considered to be outstanding learners, suggesting that immature perceptual skills might actually be advantageous to improvement on an acoustic task as a result of training (perceptual learning). Previous non‐human studies have not employed an identical task when comparing perceptual performance of young and mature subjects, making it difficult to assess learning. Here, we used an identical procedure on juvenile and adult gerbils to examine the perception of amplitude modulation (AM), a stimulus feature that is an important component of most natural sounds. On average, Adult animals could detect smaller fluctuations in amplitude (i.e., smaller modulation depths) than Juveniles, indicating immature perceptual skills in Juveniles. However, the population variance was much greater for Juveniles, a few animals displaying adult‐like AM detection. To determine whether immature perceptual skills facilitated learning, we compared naïve performance on the AM detection task with the amount of improvement following additional training. The amount of improvement in Adults correlated with naïve performance: those with the poorest naïve performance improved the most. In contrast, the naïve performance of Juveniles did not predict the amount of learning. Those Juveniles with immature AM detection thresholds did not display greater learning than Adults. Furthermore, for several of the Juveniles with adult‐like thresholds, AM detection deteriorated with repeated testing. Thus, immature perceptual skills in young animals were not associated with greater learning. © 2010 Wiley Periodicals, Inc. Develop Neurobiol 70: 636–648, 2010

A growing number of studies of auditory processing are being carried out in awake, behaving animals, creating a need for precisely controlled sound delivery without restricting head movements. We have designed a system for closed-field stimulus presentation in freely moving ferrets, which comprises lightweight, adjustable headphones that can be consistently positioned over the ears via a small, skull-mounted implant. The invasiveness of the implant was minimized by simplifying its construction and using dental adhesive only for attaching it to the skull, thereby reducing the surgery required and avoiding the use of screws or other anchoring devices. Attaching the headphones to a chronic implant also reduced the amount of contact they had with the head and ears, increasing the willingness of the animals to wear them. We validated sound stimulation via the headphones in ferrets trained previously in a free-field task to localize stimuli presented from one of two loudspeakers. Noise bursts were delivered binaurally over the headphones and interaural level differences (ILDs) were introduced to allow the sound to be lateralized. Animals rapidly transferred from the free-field task to indicate the perceived location of the stimulus presented over headphones. They showed near perfect lateralization with a 5 dB ILD, matching the scores achieved in the free-field task. As expected, the ferrets' performance declined when the ILD was reduced in value. This closed-field system can easily be adapted for use in other species, and provides a reliable means of presenting closed-field stimuli whilst monitoring behavioral responses in freely moving animals.

Background: Barn owls integrate spatial information across frequency channels to localize sounds in space. Methodology/principal findings: We presented barn owls with synchronous sounds that contained different bands of frequencies (3-5 kHz and 7-9 kHz) from different locations in space. When the owls were confronted with the conflicting localization cues from two synchronous sounds of equal level, their orienting responses were dominated by one of the sounds: they oriented toward the location of the low frequency sound when the sources were separated in azimuth; in contrast, they oriented toward the location of the high frequency sound when the sources were separated in elevation. We identified neural correlates of this behavioral effect in the optic tectum (OT, superior colliculus in mammals), which contains a map of auditory space and is involved in generating orienting movements to sounds. We found that low frequency cues dominate the representation of sound azimuth in the OT space map, whereas high frequency cues dominate the representation of sound elevation. Conclusions/significance: Significance: We argue that the dominance hierarchy of localization cues reflects several factors: 1) the relative amplitude of the sound providing the cue, 2) the resolution with which the auditory system measures the value of a cue, and 3) the spatial ambiguity in interpreting the cue. These same factors may contribute to the relative weighting of sound localization cues in other species, including humans.

Psychophysical forward masking is an increase in threshold of detection of a sound (probe) when it is preceded by another sound (masker). This is reminiscent of the reduction in neuronal responses to a sound following prior stimulation. Studies in the auditory nerve and cochlear nucleus using signal detection theory techniques to derive neuronal thresholds showed that in centrally projecting neurons, increases in masked thresholds were significantly smaller than the changes measured psychophysically. Larger threshold shifts have been reported in the inferior colliculus of awake marmoset. The present study investigated the magnitude of forward masking in primary auditory cortical neurons of anaesthetised guinea-pigs. Responses of cortical neurons to unmasked and forward masked tones were measured and probe detection thresholds estimated using signal detection theory methods. Threshold shifts were larger than in the auditory nerve, cochlear nucleus and inferior colliculus. The larger threshold shifts suggest that central, and probably cortical, processes contribute to forward masking. However, although methodological differences make comparisons difficult, the threshold shifts in cortical neurons were, in contrast to subcortical nuclei, actually larger than those observed psychophysically. Masking was largely attributable to a reduction in the responses to the probe, rather than either a persistence of the masker responses or an increase in the variability of probe responses.