Ellen Covey

Stimulus-Specific Adaptation in the Inferior Colliculus of the Anesthetized Rat

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.

Novelty detector neurons in the mammalian auditory midbrain.

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.

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.

Frequency tuning and response latencies at three levels in the brainstem of the echolocating bat, Eptesicus fuscus

To determine the level at which certain response characteristics originate, we compared monaural auditory responses of neurons in ventral cochlear nucleus, nuclei of lateral lemniscus and inferior colliculus. Characteristics examined were sharpness of frequency tuning, latency variability for individual neurons and range of latencies across neurons.Exceptionally broad tuning curves were found in the nuclei of the lateral lemniscus, while exceptionally narrow tuning curves were found in the inferior colliculus. Neither specialized tuning characteristic was found in the ventral cochlear nuclei.All neurons in the columnar division of the ventral nucleus of the lateral lemniscus maintained low variability of latency over a broad range of stimulus conditions. Some neurons in the cochlear nucleus (12%) and some in the inferior colliculus (15%) had low variability in latency but only at best frequency.Range of latencies across neurons was small in the ventral cochlear nucleus (1.3–5.7 ms), intermediate in the nuclei of the lateral lemniscus (1.7–19.8 ms) and greatest in the inferior colliculus (2.9–42.0 ms).We conclude that, in the nuclei of the lateral lemniscus and in the inferior colliculus, unique tuning and timing properties are built up from ascending inputs.

The Inferior Colliculus: A Hub for the Central Auditory System

The inferior colliculus (IC) (Fig. 7.1) occupies a strategic position in the central auditory system. Evidence reviewed in this chapter indicates that it is an interface between lower brainstem auditory pathways, the auditory cortex, and motor systems (For abbreviations see Table 7.1). The IC receives ascending input, via separate pathways, from a number of auditory nuclei in the lower brainstem. Moreover, it receives crossed input from the opposite IC and descending input from auditory cortex. These connections suggest that (1) the IC integrates information from various auditory sources and (2) at least some of the integration utilizes cortical feedback. The IC also receives input from ascending somatosensory pathways, suggesting that auditory information is integrated with somatosensory information at the midbrain. Motor-related input to the IC arises from the substantia nigra and globus pallidus. These connections raise the possibility that sensory processing in the IC is modulated by motor action. The major output of the IC is to the auditory thalamocortical system. However, it also transmits information to motor systems such as the deep superior colliculus, and the cerebellum, via the pontine gray. These connections suggest that processing in the IC not only prepares information for transmission to higher auditory centers but also modulates motor action in a direct fashion. In short, the IC is ideally suited to process auditory information based on behavioral context and to direct information for guiding action in response to this information (Aitkin 1986; Casseday and Covey 1996).

A Discontinuous Tonotopic Organization in the Inferior Colliculus of the Rat

Audible frequencies of sound are encoded in a continuous manner along the length of the cochlea, and frequency is transmitted to the brain as a representation of place on the basilar membrane. The resulting tonotopic map has been assumed to be a continuous smooth progression from low to high frequency throughout the central auditory system. Here, physiological and anatomical data show that best frequency is represented in a discontinuous manner in the inferior colliculus, the major auditory structure of the midbrain. Multiunit maps demonstrate a distinct stepwise organization in the order of best frequency progression. Furthermore, independent data from single neurons show that best frequencies at octave intervals of approximately one-third are more prevalent than others. These data suggest that, in the inferior colliculus, there is a defined space of tissue devoted to a given frequency, and input within this frequency band may be pooled for higher-level processing.

Distribution of GABAA, GABAB, and glycine receptors in the central auditory system of the big brown bat, Eptesicus fuscus

Quantitative autoradiographic techniques were used to compare the distribution of GABAA, GABAB, and glycine receptors in the subcortical auditory pathway of the big brown bat, Eptesicus fuscus. For GABAA receptors, the ligand used was 35S‐t‐butylbicyclophosphorothionate (TBPS); for GABAB receptors, 3H‐GABA was used as a ligand in the presence of isoguvacine to block binding to GABAA sites; for glycine, the ligand used was 3H‐strychnine. In the subcortical auditory nuclei there appears to be at least a partial complementarity in the distribution of GABAA receptors labeled with 35S‐TBPS and glycine receptors labeled with 3H‐strychnine. GABAA receptors were concentrated mainly in the inferior colliculus (IC) and medial geniculate nucleus, whereas glycine receptors were concentrated mainly in nuclei below the level of the IC. Within the IC, there was a graded spatial distribution of 35S‐TBPS binding; the most dense labeling was in the dorsomedial region, but very sparse labeling was observed in the ventrolateral region. There was also a graded spatial distribution of 3H‐strychnine binding. The most dense labeling was in the ventral and lateral regions and the weakest labeling was in the dorsomedial region. Thus, in the IC, the distribution of 35S‐TBPS was complementary to that of 3H‐strychnine. GABAB receptors were distributed at a low level throughout the subcortical auditory nuclei, but were most prominent in the dorsomedial part of the IC.

The Lower Brainstem Auditory Pathways

In the auditory system, more than any other sensory modality, extensive processing of incoming signals occurs in the brainstem. In all vertebrates, the auditory pathways below the inferior colliculus consist of a complex system of parallel pathways, each with its own centers for signal processing. The auditory structures of the lower brainstem act as filters to selectively enhance specific stimulus features and as computational centers to add, subtract, or compare signals in different channels. Some brainstem structures, such as the superior olive, have been studied extensively, and their function is at least partially understood. Others, such as the nuclei of the lateral lemniscus, have been largely ignored, and their functional roles are just beginning to be discovered.

The columnar region of the ventral nucleus of the lateral lemniscus in the big brown bat (Eptesicus fuscus): synaptic arrangements and structural correlates of feedforward inhibitory function

Abstract.Neurons of the columnar region of the ventral nucleus of the lateral lemniscus of Eptesicus fuscus respond with high-precision constant-latency responses to sound onsets and possess remarkably broad tuning. To study the synaptic basis for this specialized monaural auditory processing and to elucidate the excitatory or inhibitory nature of the input and output circuitry, we have used classical transmission electron microscopy, and postembedding immunocytochemistry for gamma aminobutyric acid (GABA) and glycine on serial semithin sections. The dominant putatively excitatory perisomatic input is provided by large calyx-like terminals that possess round synaptic vesicles and asymmetric synaptic contacts. Additionally, calyces contact the dendrites of neighboring neurons. Putatively inhibitory small boutons possess pleomorphic or flattened synaptic vesicles and symmetrical contacts and are sparsely distributed on somata and dendrites. Almost all neurons are glycine-immunoreactive. There is a moderate amount of glycine-immunoreactive puncta; GABA-immunoreactive puncta are rare. This suggests that (1) there is a fast robust excitatory synaptic input via calyx-like perisomatic endings, (2) calyx-like endings distribute frequency-specific excitatory input across isofrequency sheets by virtue of parallel synapses to somata and adjacent dendrites, and thus, dendritic integration may contribute to the broadening of frequency tuning, (3) the columnar region forms an inhibitory glycinergic feedforward relay in the ascending auditory pathway, a relay that is probably involved in creating filters for time-varying signals.

On the singularity of taste sensations: What is a taste primary?

Abstract It is commonly accepted that there are four primary tastes. This conceptualization is notable for its simplicity and usefulness in guiding research and organizing data in the stimulus, receptor, neural and psychophysical aspects of taste. But however strongly defended or widely used, the concept of a primary taste remains undefined, especially in the psychophysical sense. The present research sets forth and tests one psychophysical defining property of a taste primary, that it should appear singular, and remain singular when mixed with other tastes; i.e., several singular tastes, when mixed, should remain separate and distinct. It is shown that mixtures are often judged to be as singular as their separate components, indicating synthesis of new tastes different from the components, and thus the existence of more than the few primary tastes.