Electrophysiology publications

The ability to detect novel sounds in a complex acoustic context is crucial for survival. Neurons from midbrain through cortical levels adapt to repetitive stimuli, while maintaining responsiveness to rare stimuli, a phenomenon called stimulus-specific adaptation (SSA). The site of origin and mechanism of SSA are currently unknown. We used microiontophoretic application of gabazine to examine the role of GABA(A)-mediated inhibition in SSA in the inferior colliculus, the midbrain center for auditory processing. We found that gabazine slowed down the process of adaptation to high probability stimuli but did not abolish it, with response magnitude and latency still depending on the probability of the stimulus. Blocking GABA(A) receptors increased the firing rate to high and low probability stimuli, but did not completely equalize the responses. Together, these findings suggest that GABA(A)-mediated inhibition acts as a gain control mechanism that enhances SSA by modifying the responsiveness of the neuron.

Stimulus-specific adaptation (SSA) is the ability of some neurons to respond better to rare than to frequent, repetitive stimuli. In the auditory system, SSA has been found at the level of the midbrain, thalamus, and cortex. While previous studies have used the whole overall neuronal response to characterize SSA, here we present a detailed analysis on the variations within the time course of the evoked responses. The extracellular activity of well isolated single neurons from the inferior colliculus (IC) was recorded during stimulation using an oddball paradigm, which is able to elicit SSA. At the same time, these responses were evaluated before, during, and after the microiontophoretic application of gabazine, a specific antagonist of GABA(A) receptors, to study the contribution of inhibition to the responses of these neurons. We then analyzed the difference signal (DS), which is the difference in the PSTH in response to rare and frequent stimuli. We found that, even in a sample of neurons showing strong SSA (i.e., showing larger preference for rare stimuli), the DS was variable and one third of the neurons contained portions that responded significantly better to the frequent stimuli than to the rare. This variability is not observed when averaging the responses of multiple cells. Furthermore, the blockade of GABA(A) receptors increased the number of neurons showing portions that responded better to the frequent stimuli, indicating that inhibition in the IC refines and sharpens SSA in the neural responses.

The auditory pathways coursing through the brainstem are organized bilaterally in mirror image about the midline and at several levels the two sides are interconnected. One of the most prominent points of interconnection is the commissure of the inferior colliculus (CoIC). Anatomical studies have revealed that these fibers make reciprocal connections which follow the tonotopic organization of the inferior colliculus (IC), and that the commissure contains both excitatory and, albeit fewer, inhibitory fibers. The role of these connections in sound processing is largely unknown. Here we describe a method to address this question in the anaesthetized guinea pig. We used a cryoloop placed on one IC to produce reversible deactivation while recording electrophysiological responses to sounds in both ICs. We recorded single units, multi-unit clusters and local field potentials (LFPs) before, during and after cooling. The degree and spread of cooling was measured with a thermocouple placed in the IC and other auditory structures. Cooling sufficient to eliminate firing was restricted to the IC contacted by the cryoloop. The temperature of other auditory brainstem structures, including the contralateral IC and the cochlea were minimally affected. Cooling below 20°C reduced or eliminated the firing of action potentials in frequency laminae at depths corresponding to characteristic frequencies up to ~8 kHz. Modulation of neural activity also occurred in the un-cooled IC with changes in single unit firing and LFPs. Components of LFPs signaling lemniscal afferent input to the IC showed little change in amplitude or latency with cooling, whereas the later components, which likely reflect inter- and intra-collicular processing, showed marked changes in form and amplitude. We conclude that the cryoloop is an effective method of selectively deactivating one IC in guinea pig, and demonstrate that auditory processing in the IC is strongly influenced by the other.

Background: Sound production and hearing sensitivity of ectothermic animals are affected by the ambient temperature. This is the first study investigating the influence of temperature on both sound production and on hearing abilities in a fish species, namely the neotropical Striped Raphael catfish Platydoras armatulus. Methodology/principal findings: Doradid catfishes produce stridulation sounds by rubbing the pectoral spines in the shoulder girdle and drumming sounds by an elastic spring mechanism which vibrates the swimbladder. Eight fish were acclimated for at least three weeks to 22°, then to 30° and again to 22°C. Sounds were recorded in distress situations when fish were hand-held. The stridulation sounds became shorter at the higher temperature, whereas pulse number, maximum pulse period and sound pressure level did not change with temperature. The dominant frequency increased when the temperature was raised to 30°C and the minimum pulse period became longer when the temperature decreased again. The fundamental frequency of drumming sounds increased at the higher temperature. Using the auditory evoked potential (AEP) recording technique, the hearing thresholds were tested at six different frequencies from 0.1 to 4 kHz. The temporal resolution was determined by analyzing the minimum resolvable click period (0.3-5 ms). The hearing sensitivity was higher at the higher temperature and differences were more pronounced at higher frequencies. In general, latencies of AEPs in response to single clicks became shorter at the higher temperature, whereas temporal resolution in response to double-clicks did not change. Conclusions/significance: These data indicate that sound characteristics as well as hearing abilities are affected by temperatures in fishes. Constraints imposed on hearing sensitivity at different temperatures cannot be compensated even by longer acclimation periods. These changes in sound production and detection suggest that acoustic orientation and communication are affected by temperature changes in the neotropical catfish P. armatulus.

Interaural time differences (ITDs) are the major cue for localizing low-frequency sounds. The activity of neuronal populations in the brainstem encodes ITDs with an exquisite temporal acuity of about 10 μs. The response of single neurons, however, also changes with other stimulus properties like the spectral composition of sound. The influence of stimulus frequency is very different across neurons and thus it is unclear how ITDs are encoded independently of stimulus frequency by populations of neurons. Here we fitted a statistical model to single-cell rate responses of the dorsal nucleus of the lateral lemniscus. The model was used to evaluate the impact of single-cell response characteristics on the frequency-invariant mutual information between rate response and ITD. We found a rough correspondence between the measured cell characteristics and those predicted by computing mutual information. Furthermore, we studied two readout mechanisms, a linear classifier and a two-channel rate difference decoder. The latter turned out to be better suited to decode the population patterns obtained from the fitted model.

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 directionality of hair cell stimulation combined with the vibration of the basilar membrane causes the auditory nerve fiber action potentials, in response to low-frequency stimuli, to occur at a particular phase of the stimulus waveform. Because direct mechanical measurements at the cochlear apex are difficult, such phase locking has often been used to indirectly infer the basilar membrane motion. Here, we confirm and extend earlier data from mammals using sine wave stimulation over a wide range of sound levels (up to 90 dB sound pressure level). We recorded phase-locked responses to pure tones over a wide range of frequencies and sound levels of a large population of auditory nerve fibers in the anesthetized guinea pig. The results indicate that, for a constant frequency of stimulation, the phase lag decreases with increases in the characteristic frequency (CF) of the nerve fiber. The phase lag decreases up to a CF above the stimulation frequency, beyond which it decreases at a much slower rate. Such phase changes are consistent with known basal cochlear mechanics. Measurements from individual fibers showed smaller but systematic variations in phase with sound level, confirming previous reports. We found a "null" stimulation frequency at which little variation in phase occurred with sound level. This null frequency was often not at the CF. At stimulation frequencies below the null, there was a progressive lag with sound level and a progressive lead for stimulation frequencies above the null. This was maximally 0.2 cycles.