Neural Mechanisms for Spectral Analysis in the Auditory Midbrain, Thalamus, and Cortex

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This chapter examines the principles of spectral analysis and coding in the ascending central auditory system. The identifying key response properties of single neurons in the lemniscal divisions of the inferior colliculus (ICC), auditory thalamus (MGBv), and primary auditory cortex (AI) that can be related to the underlying anatomical architecture in these stations, are discussed. Starting with the divergent pathway from the cochlea to the brainstem nuclei, the ICC receives input from the cochlear nucleus (CN), superior olivary nuclei (SO), and the nucleus of the lateral lemniscus (NLL). This convergent pattern of innervating input from multiple brainstem nuclei plays a key role in refining the organization of spectral and temporal preferences in the ICC. The chapter explains the general principles of coding that serve as a functional and anatomical substrate for spectral analysis in the central auditory system, and also focuses on relating details of a single neuron activity to the underlying anatomical layout and connectivity at different levels of the lemniscal auditory pathway. Spectral response properties and selectivity are intimately related to binaural preferences and sound level dependence. The chapter further explores the specific relationships between different response attributes and the underlying local circuitry and global organization of the central auditory system. General properties of single neuron sensitivities are outlined whereas their relationship to the anatomical circuitry and the underlying functional transformation is described.

Introduction

This chapter examines the principles of spectral analysis and coding in the ascending central auditory system. The chapter is centered around identifying key response properties of single neurons in the lemniscal divisions of the inferior colliculus (ICC), auditory thalamus (MGBv), and primary auditory cortex (AI) that can be related to the underlying anatomical architecture in these stations. Starting with the divergent pathway from the cochlea to the brainstem nuclei, the ICC receives input from the cochlear nucleus (CN), superior olivary nuclei (SO), and the nucleus of the lateral lemniscus (NLL) (Adams, 1979). This highly convergent pattern of innervating input from multiple brainstem nuclei plays a key role in refining the organization of spectral and temporal preferences in the ICC. Within this context, spectral and temporal preferences in the ICC are sequentially modified in the thalamus and cortex leading to distinct differences in the functional organization. This functional and anatomical framework is essential for understanding the distributed code for spectral and temporal features in a sound.

The chapter emphasizes the general principles of coding which serve as a functional and anatomical substrate for spectral analysis in the central auditory system. In particular, we focus on relating details of single neuron activity to the underlying anatomical layout and connectivity at different levels of the lemniscal auditory pathway. Spectral response properties and selectivity are intimately related to binaural preferences and sound level dependence. Throughout we explore the specific relationships between these different response attributes and the underlying local circuitry and global organization of the central auditory system. General properties of single neuron sensitivities are outlined in II Principles of Spectral Analysis in ICC, MGB, and AI, III Sharpness of Tuning, Bandwidth, and Level Dependence, IV Excitatory and Inhibitory Receptive Field Properties, V Spectral and Temporal Integration whereas their relationship to the anatomical circuitry and the underlying functional transformation is described in VI Organization of Spectral Receptive Field Properties in Neuronal Populations of ICC, MGBv, and AI, VII Primary Auditory Cortical Acoustic Feature Representation and Processing, VIII Physiologic Distinctions or Transformations in AI.

Section snippets

Principles of Spectral Analysis in ICC, MGB, and AI

The frequency organization of the cochlear sensory epithelium is conserved in the topographic pattern of neuronal frequency selectivities or cochleotopy. A cochleotopic pattern of frequency response properties is observed throughout the lemniscal auditory pathway including the ICC, MGBv, and AI. Demonstrating the functional consequences associated with specific anatomical patterns of frequency specific projections in the lemniscal pathway requires efficient and meaningful ways of characterizing

Sharpness of Tuning, Bandwidth, and Level Dependence

Frequency and absolute sound level are important attributes in complex sounds that are known to influence perception. The spectrum of communication sounds and other behaviorally relevant environmental signals can vary significantly in their frequency content and amplitude level. Frequency content, disparity in frequency composition for the two ears, and absolute sound level can also encode for the location of sound sources. It is the task of the central auditory system to faithfully represent

Excitatory and Inhibitory Receptive Field Properties

Inhibitory processes are initially established early on in the CN (Davis and Young, 2000), and further refined at more central centers. Feed‐forward inhibitory projections from multiple auditory centers play a prominent role in shaping spectral sensitivities. This receptive field shaping could occur via long range tonotopically organized inhibitory projections from the dorsal nucleus of the lateral lemniscus (DNLL) to the ICC (Bajo 1999, Oliver 1989, Pollak 2002, Pollak 2003, Shneiderman 1989,

Spectral and Temporal Integration

Timing differences in the delay and duration of neuronal excitation and inhibition have a significant impact on the way a neuron responds to a dynamic stimulus. The temporal response pattern of a neuron is not only dependent on the spectral content of a sound but is also affected by the temporal evolution of the stimulus. Neurons in the DCN and beyond are selective for the spectro‐temporal content of the sound.

Inhibition shapes spectral selectivity and also refines temporal aspects of the

Organization of Spectral Receptive Field Properties in Neuronal Populations of ICC, MGBv, and AI

In order to appreciate the transformations in spectral receptive field properties at each successive stage of the auditory sensory pathway, it is important to recognize that there are many processes that serve to alter frequency encoding in the peripheral sensory system. There are at least three anatomically and functionally distinct branches of the lemniscal pathway ascending from the periphery to the auditory brainstem. Indeed, some have suggested more (Thompson and Schofield, 2000). These

Primary Auditory Cortical Acoustic Feature Representation and Processing

Auditory cortex can be sub‐divided according to cochleotopic organization, spectral integration, azimuth tuning properties, and behavioral effects following lesions. Up to four distinct cochleotopically organized regions have been described in mammalian auditory cortex (Schreiner et al., 2000). Examples of differences in cochleotopic representations are described in the following text and illustrated in part in Fig. 8. A direct correlation between the cochleotopy and specializations in spectral

Level‐Dependent Broad Bandwidth Azimuth Tuning

A correspondence between level‐dependence and sound source location tuning appears for the first time in AI. Azimuth‐tuned neurons in MGBv and AI have non‐monotonic level‐dependent responses to broadband noise; however, the level dependence is greater for AI (Barone 1996, Clarey 1995). At the levels of DCN and MGBv there is no correlation between level dependence and azimuth tuning (Barone et al., 1996). Azimuth tuning also becomes sharper in AI relative to MGBv (Barone 1996, Samson 2000).

Conclusions

Demonstrating the distinct spectral processing streams in the lemniscal auditory pathway has been a formidable task and yet we still do not fully understand their functional role in sound perception. Perhaps the most fundamental task of the cochlea and the lemniscal auditory pathway as a whole is to decompose sounds into frequency channels that can be further analyzed and processed in central stations. Still, numerous aspects of the functional and organizational principles in central auditory

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