K. Jannis Hildebrandt

The Origin of Adaptation in the Auditory Pathway of Locusts Is Specific to Cell Type and Function

We investigated the origin of spike frequency adaptation within a layered sensory network: the auditory pathway of locusts. Spike frequency adaptation as observed in an individual neuron may arise because of intrinsic or presynaptic adaptation mechanisms. To separate the contribution of different mechanisms, we recorded from the same cell during acoustic and intracellular current stimulation. We studied three identified neuron types that are representative for each network layer and participate in processing auditory patterns and localizing sound sources. By comparing current and acoustic stimulation, three distinct patterns of the distribution of adaptation mechanisms within the sensory network emerged: (1) balanced influence of both intrinsic and presynaptic adaptation mechanisms in an interneuron that summates over several receptor afferents (TN1), (2) predominantly inhibiting input as the source for spike frequency adaptation in a cell that transmits both pattern representation and directional information (BSN1), (3) primarily intrinsic, spike-triggered adaptation currents within an interneuron coding exclusively for direction (AN2). The time courses of spike frequency adaptation differed significantly between the cells types. Using the adaptation time constants, we were able to predict signal transmission properties for the different cells. We conclude that the adaptation mechanisms differ greatly among interneurons within this sensory pathway and are a function of their role in information processing.

Computational themes of peripheral processing in the auditory pathway of insects

Hearing in insects serves to gain information in the context of mate finding, predator avoidance or host localization. For these goals, the auditory pathways of insects represent the computational substrate for object recognition and localization. Before these higher level computations can be executed in more central parts of the nervous system, the signals need to be preprocessed in the auditory periphery. Here, we review peripheral preprocessing along four computational themes rather than discussing specific physiological mechanisms: (1) control of sensitivity by adaptation, (2) recoding of amplitude modulations of an acoustic signal into a labeled-line code (3) frequency processing and (4) conditioning for binaural processing. Along these lines, we review evidence for canonical computations carried out in the peripheral auditory pathway and show that despite the vast diversity of insect hearing, signal processing is governed by common computational motifs and principles.

Neural maps in insect versus vertebrate auditory systems

The convergent evolution of hearing in insects and vertebrates raises the question about similarity of the central representation of sound in these distant animal groups. Topographic representations of spectral, spatial and temporal cues have been widely described in mammals, but evidence for such maps is scarce in insects. Recent data on insect sound encoding provides evidence for an early integration of sound parameters to form highly-specific representation that predict behavioral output. In mammals, new studies investigating neural representation of perceptual features in behaving animals allow asking similar questions. A comparative approach may help in understanding principles underlying the formation of perceptual categories and behavioral plasticity.

Adaptation and Selective Information Transmission in the Cricket Auditory Neuron AN2

Sensory systems adapt their neural code to changes in the sensory environment, often on multiple time scales. Here, we report a new form of adaptation in a first-order auditory interneuron (AN2) of crickets. We characterize the response of the AN2 neuron to amplitude-modulated sound stimuli and find that adaptation shifts the stimulus–response curves toward higher stimulus intensities, with a time constant of 1.5 s for adaptation and recovery. The spike responses were thus reduced for low-intensity sounds. We then address the question whether adaptation leads to an improvement of the signals representation and compare the experimental results with the predictions of two competing hypotheses: infomax, which predicts that information conveyed about the entire signal range should be maximized, and selective coding, which predicts that “foreground” signals should be enhanced while “background” signals should be selectively suppressed. We test how adaptation changes the input–response curve when presenting signals with two or three peaks in their amplitude distributions, for which selective coding and infomax predict conflicting changes. By means of Bayesian data analysis, we quantify the shifts of the measured response curves and also find a slight reduction of their slopes. These decreases in slopes are smaller, and the absolute response thresholds are higher than those predicted by infomax. Most remarkably, and in contrast to the infomax principle, adaptation actually reduces the amount of encoded information when considering the whole range of input signals. The response curve changes are also not consistent with the selective coding hypothesis, because the amount of information conveyed about the loudest part of the signal does not increase as predicted but remains nearly constant. Less information is transmitted about signals with lower intensity.

A neural mechanism for time-window separation resolves ambiguity of adaptive coding.

The senses of animals are confronted with changing environments and different contexts. Neural adaptation is one important tool to adjust sensitivity to varying intensity ranges. For instance, in a quiet night outdoors, our hearing is more sensitive than when we are confronted with the plurality of sounds in a large city during the day. However, adaptation also removes available information on absolute sound levels and may thus cause ambiguity. Experimental data on the trade-off between benefits and loss through adaptation is scarce and very few mechanisms have been proposed to resolve it. We present an example where adaptation is beneficial for one task—namely, the reliable encoding of the pattern of an acoustic signal—but detrimental for another—the localization of the same acoustic stimulus. With a combination of neurophysiological data, modeling, and behavioral tests, we show that adaptation in the periphery of the auditory pathway of grasshoppers enables intensity-invariant coding of amplitude modulations, but at the same time, degrades information available for sound localization. We demonstrate how focusing the response of localization neurons to the onset of relevant signals separates processing of localization and pattern information temporally. In this way, the ambiguity of adaptive coding can be circumvented and both absolute and relative levels can be processed using the same set of peripheral neurons.

The Impact of Anesthetic State on Spike-Sorting Success in the Cortex: A Comparison of Ketamine and Urethane Anesthesia

Spike sorting is an essential first step in most analyses of extracellular in vivo electrophysiological recordings. Here we show that spike-sorting success depends critically on characteristics of coordinated population activity that can differ between anesthetic states. In tetrode recordings from mouse auditory cortex, spike sorting was significantly less successful under ketamine/medetomidine (ket/med) than urethane anesthesia. Surprisingly, this difficulty with sorting under ket/med anesthesia did not appear to result from either greater millisecond-scale burstiness of neural activity or increased coordination of activity among neighboring neurons. Rather, the key factor affecting sorting success appeared to be the amount of coordinated population activity at long time intervals and across large cortical distances. We propose that spike-sorting success is directly dependent on overall coordination of activity, and is most disrupted by large-scale fluctuations in cortical population activity. Reliability of single-unit recording may therefore differ not only between urethane-anesthetized and ket/med-anesthetized states as demonstrated here, but also between synchronized and desynchronized states, asleep and awake states, or inattentive and attentive states in unanesthetized animals.

Context-dependent coding and gain control in the auditory system of crickets

Sensory systems process stimuli that greatly vary in intensity and complexity. To maintain efficient information transmission, neural systems need to adjust their properties to these different sensory contexts, yielding adaptive or stimulus‐dependent codes. Here, we demonstrated adaptive spectrotemporal tuning in a small neural network, i.e. the peripheral auditory system of the cricket. We found that tuning of cricket auditory neurons was sharper for complex multi‐band than for simple single‐band stimuli. Information theoretical considerations revealed that this sharpening improved information transmission by separating the neural representations of individual stimulus components. A network model inspired by the structure of the cricket auditory system suggested two putative mechanisms underlying this adaptive tuning: a saturating peripheral nonlinearity could change the spectral tuning, whereas broad feed‐forward inhibition was able to reproduce the observed adaptive sharpening of temporal tuning. Our study revealed a surprisingly dynamic code usually found in more complex nervous systems and suggested that stimulus‐dependent codes could be implemented using common neural computations.

Ultra-fine temporal resolution in auditory processing is preserved in aged mice without peripheral hearing loss

Age-related hearing loss (presbycusis) is caused by damage to the periphery as well as deterioration of central auditory processing. Gap detection is a paradigm to study age-related temporal processing deficits, which is assumed to be determined primarily by the latter. However, peripheral hearing loss is a strong confounding factor when using gap detection to measure temporal processing. In this study, we used mice from the CAST line, which is known to maintain excellent peripheral hearing, to rule out any contribution of peripheral hearing loss to gap detection performance. We employed an operant Go/No-go paradigm to obtain psychometric functions of gap in noise (GIN) detection at young and middle age. Besides, we measured auditory brainstem responses (ABR) and multiunit recordings in the auditory cortex (AC) in order to disentangle the processing stages of gap detection. We found detection thresholds around 0.6 ms in all measurement modalities. Detection thresholds did not increase with age. In the ABR, GIN stimuli are coded as onset responses to the noise that follows the gap, strikingly similar to the ABR of noise bursts in silence (NBIS). The simplicity of the neural representation of the gap together with the preservation of detection threshold in aged CAST mice suggests that GIN detection in the mouse is primarily determined by peripheral, not central processing. Abbreviaions GIN gap in noise ABR auditory brainstem response AC auditory cortex NBIS noise burst in silence IIN inhibitory interneuron

Effects of Exogenous Auditory Attention on Temporal and Spectral Resolution

Previous research in the visual domain suggests that exogenous attention in form of peripheral cueing increases spatial but lowers temporal resolution. It is unclear whether this effect transfers to other sensory modalities. Here, we tested the effects of exogenous attention on temporal and spectral resolution in the auditory domain. Eighteen young, normal-hearing adults were tested in both gap and frequency change detection tasks with exogenous cuing. Benefits of valid cuing were only present in the gap detection task while costs of invalid cuing were observed in both tasks. Our results suggest that exogenous attention in the auditory system improves temporal resolution without compromising spectral resolution.

Electrical stimulation of the midbrain excites the auditory cortex asymmetrically

BACKGROUND Auditory midbrain implant users cannot achieve open speech perception and have limited frequency resolution. It remains unclear whether the spread of excitation contributes to this issue and how much it can be compensated by current-focusing, which is an effective approach in cochlear implants. OBJECTIVE The present study examined the spread of excitation in the cortex elicited by electric midbrain stimulation. We further tested whether current-focusing via bipolar and tripolar stimulation is effective with electric midbrain stimulation and whether these modes hold any advantage over monopolar stimulation also in conditions when the stimulation electrodes are in direct contact with the target tissue. METHODS Using penetrating multielectrode arrays, we recorded cortical population responses to single pulse electric midbrain stimulation in 10 ketamine/xylazine anesthetized mice. We compared monopolar, bipolar, and tripolar stimulation configurations with regard to the spread of excitation and the characteristic frequency difference between the stimulation/recording electrodes. RESULTS The cortical responses were distributed asymmetrically around the characteristic frequency of the stimulated midbrain region with a strong activation in regions tuned up to one octave higher. We found no significant differences between monopolar, bipolar, and tripolar stimulation in threshold, evoked firing rate, or dynamic range. CONCLUSION The cortical responses to electric midbrain stimulation are biased towards higher tonotopic frequencies. Current-focusing is not effective in direct contact electrical stimulation. Electrode maps should account for the asymmetrical spread of excitation when fitting auditory midbrain implants by shifting the frequency-bands downward and stimulating as dorsally as possible.