Deciphering the brain's codes

The two sensory systems discussed use similar algorithms for the synthesis of the neuronal selectivity for the stimulus that releases a particular behavior, although the neural circuits, the brain sites involved, and even the species are different. This stimulus selectivity emerges gradually in a neural network organized according to parallel and hierarchical design principles. The parallel channels contain lower order stations with special circuits for the creation of neuronal selectivities for different features of the stimulus. Convergence of the parallel pathways brings these selectivities together at a higher order station for the eventual synthesis of the selectivity for the whole stimulus pattern. The neurons that are selective for the stimulus are at the top of the hierarchy, and they form the interface between the sensory and motor systems or between sensory systems of different modalities. The similarities of these two systems at the level of algorithms suggest the existence of rules of signal processing that transcend different sensory systems and species of animals

Binaural characteristics of units in the owl's brainstem auditory pathway: precursors of restricted spatial receptive fields

The barn owl uses binaural phase and intensity differences for sound localization. These two cues also determine the receptive fields of specialized neurons in the inferior colliculus. The main aim of this study was to investigate where neuronal sensitivity to the binaural cues emerges in the brainstem auditory nuclei, and how this sensitivity reaches the neurons in the inferior colliculus. The owl's phase- sensitive neurons are selective to microsecond phase differences of high frequency signals, unlike mammalian phase-sensitive neurons which are restricted to low frequency signals. In certain nuclei virtually all of the neurons are sensitive to either phase differences or intensity differences, but not to both. These nuclei form two distinctly separate pathways that converge at the inferior colliculus where neurons selective to both phase and intensity differences occur. In contrast to the mammalian auditory system, the owl's phase- and intensity difference-sensitive pathways are not segregated into low frequency and high frequency channels

The Role of GABAergic Inhibition in Processing of lnteraural Time Difference in the Owl's Auditory System

The barn owl uses interaural time differences (ITDs) to localize the azimuthal position of sound. ITDs are processed by an anatomically distinct pathway in the brainstem. Neuronal selectivity for ITD is generated in the nucleus laminaris (NL) and conveyed to both the anterior portion of the ventral nucleus of the lateral lemniscus (VLVa) and the central (ICc) and external (ICx) nuclei of the inferior colliculus. With tonal stimuli, neurons in all regions are found to respond maximally not only to the real ITD, but also to ITDs that differ by integer multiples of the tonal period. This phenomenon, phase ambiguity, does not occur when ICx neurons are stimulated with noise. The main aim of this study was to determine the role of GABAergic inhibition in the processing of ITDs. Selectivity for ITD is similar in the NL and VLVa and improves in the ICc and ICx. Iontophoresis of bicuculline methiodide (BMI), a selective GABAA antagonist, decreased the ITD selectivity of ICc and ICx neurons, but did not affect that of VLVa neurons. Responses of VLVa and ICc neurons to unfavorable ITDs were below the monaural response levels. BMI raised both binaural responses to unfavorable ITDs and monaural responses, though the former remained smaller than the latter. During BMI application, ICx neurons showed phase ambiguity to noise stimuli and no longer responded to a unique ITD. BMI increased the response magnitude and changed the temporal discharge patterns in the VLVa, ICc, and ICx. Iontophoretically applied GABA exerted effects opposite to those of BMI, and the effects could be antagonized with simultaneous application of BMI. These results suggest that GABAergic inhibition (1) sharpens ITD selectivity in the ICc and ICx, (2) contributes to the elimination of phase ambiguity in the ICx, and (3) controls response magnitude and temporal characteristics in the VLVa, ICc, and ICx. Through these actions, GABAergic inhibition shapes the horizontal dimension of the auditory receptive fields

Selectivity for lnteraural Time Difference in the Owl's Midbrain

The barn owl uses the interaural difference in the timing of sounds to determine the azimuth of the source. When the sound has a wide frequency band, localization is precise. When localizing tones, however, the barn owl errs in a manner that suggests that it is confused by phantom targets. We report a neural equivalent of these phenomena as they are observed in the space-specific neuron of the owl's inferior colliculus. When stimulated with a tone, the space- specific neuron discharges maximally at interaural time differences (ITDs) that differ by one period of the stimulus tone. Changing the stimulus frequency changes the period of the ITD-response functions, but 1 ITD evokes, in most neurons, a maximal response, regardless of frequency. This ITD is the characteristic delay (CD). When stimulated with noise, there is a maximal response only to ITDs at or near the CD. Thus, the space-specific neuron can unambiguously signal the CD, provided that the signal contains more than 1 frequency. The preferential response to a single ITD, which is observed with noise stimuli, was also observed when the summed waveform of the best frequency and another tone, F2, was presented. The response of the space-specific neuron to these 2-tone stimuli could not be accounted for by the summing or averaging of the ITD-response functions obtained with the best frequency or F2 alone, suggesting that nonlinear neural processes are involved

A Neural Map of Interaural Intensity Differences in the Brain Stem of the Barn Owl

The nucleus ventralis lemnisci lateralis pars posterior (VLVp) is the first binaural station in the intensity-processing pathway of the barn owl. Contralateral stimulation excites and ipsilateral stimulation inhibits VLVp cells. The strength of the inhibition declines systematically from dorsal to ventral within the nucleus. Cells selective for different intensity disparities occur in an orderly sequence from dorsal to ventral within each isofrequency lamina. Cells at intermediate depths in the nucleus are selective for a particular narrow range of interaural intensity differences independently of the absolute sound-pressure level. A simple model of the interaction between inhibition and excitation can explain most of the response properties of VLVp neurons. The map of selectivity for intensity disparity is mainly based on the gradient of inhibition

Neuromorphic object localization using resistive memories and ultrasonic transducers

Real-world sensory-processing applications require compact, low-latency, and low-power computing systems. Enabled by their in-memory event-driven computing abilities, hybrid memristive-Complementary Metal-Oxide Semiconductor neuromorphic architectures provide an ideal hardware substrate for such tasks. To demonstrate the full potential of such systems, we propose and experimentally demonstrate an end-to-end sensory processing solution for a real-world object localization application. Drawing inspiration from the barn owl’s neuroanatomy, we developed a bio-inspired, event-driven object localization system that couples state-of-the-art piezoelectric micromachined ultrasound transducer sensors to a neuromorphic resistive memories-based computational map. We present measurement results from the fabricated system comprising resistive memories-based coincidence detectors, delay line circuits, and a full-custom ultrasound sensor. We use these experimental results to calibrate our system-level simulations. These simulations are then used to estimate the angular resolution and energy efficiency of the object localization model. The results reveal the potential of our approach, evaluated in orders of magnitude greater energy efficiency than a microcontroller performing the same task

Representation of lnteraural Time Difference in the Central Nucleus of the Barn Owl's Inferior Colliculus

This paper investigates the role of the central nucleus of the barn owl's inferior colliculus in determination of the sound-source azimuth. The central nucleus contains many neurons that are sensitive to interaural time difference (ITD), the cue for azimuth in the barn owl. The response of these neurons varies in a cyclic manner with the ITD of a tone or noise burst. Response maxima recur at integer multiples of the period of the stimulating tone, or, if the stimulus is noise, at integer multiples of the period corresponding to the neuron's best frequency. Such neurons can signal, by means of their relative spike rate, the phase difference between the sounds reaching the left and right ears. Since an interaural phase difference corresponds to more than one ITD, these neurons represent ITD ambiguously. We call this phenomenon phase ambiguity. The central nucleus is tonotopically organized and its neurons are narrowly tuned to frequency. Neurons in an array perpendicular to isofrequency laminae form a physiological and anatomical unit; only one ITD, the array-specific ITD, activates all neurons in an array at the same relative level. We, therefore, may say that, in the central nucleus, an ITD is conserved in an array of neurons. Array-specific ITDs are mapped and encompass the entire auditory space of the barn owl. Individual space-specific neurons of the external nucleus, which receive inputs from a wide range of frequency channels (Knudsen and Konishi, 1978), are selective for a unique ITD. Space-specific neurons do not show phase ambiguity when stimulated with noise (Takahashi and Konishi, 1986). Space-specific neurons receive inputs from arrays that are selective for the same ITD. The collective response of the neurons in an array may be the basis for the absence of phase ambiguity in space-specific neurons

A Comparative Study on the Modulatory Effects of Inhibition in the Mammalian and Avian Sound Localization Circuits

Sound localization is a critically important task for many animals including humans. Due to physical constraints acting on the circuits that process sound localization cues, many neural specializations have evolved. One of the key features and the focus of this dissertation is inhibitory input. To assess the impact of inhibition, I employ in vitro patch clamp techniques to observe cellular and synaptic physiology in brainstem circuits dedicated to sound localization processing. Using a mammalian model, I test the impact that GABAB receptor (GABABR) activation has on the inputs to the medial superior olive (MSO), the first area where sound localization computations take place. Activation of GABABRs modulates both excitatory and inhibitory inputs such that the magnitude of these inputs is decreased and the time course of inhibitory inputs is slowed. The functional significance of this modulation was tested using a bilateral stimulation protocol, which simulates the coincidence of in vivo excitatory inputs. Here, activation of GABABRs increased the sensitivity of MSO neurons to simulated interaural time disparity (ITD), the main cue for low frequency sound localization. To expand on these results, a computational model was used to show that each GABABR dependent modulation had a beneficial impact on ITD sensitivity in the MSO. In an avian system, I described the synaptic activity involving the superior olivary nucleus (SON), which provides the main inhibitory input in the avian sound localization circuit. At the SON itself, synaptic transmission consists of both GABA- and glycinergic components where glycine release is the result of co-release with GABA. I also show that functional glycine receptors localize at brainstem nuclei and that high frequency stimulation results in the release glycine onto nucleus magnocellularis neurons, a feature of the avian brainstem that has not been observed previously. In related experiments, I evaluate possible interactions that may occur when both GABA and glycine receptor systems are activated simultaneously. Here, a pre-activation of GlyRs leads the a decrease in conductance through the GABAAR likely due to changes in Cl- ion concentrations which manipulate the driving force of the ion