Heather L. Read

Functional Convergence of Response Properties in the Auditory Thalamocortical System

One of the brains fundamental tasks is to construct and transform representations of an animals environment, yet few studies describe how individual neurons accomplish this. Our results from correlated pairs in the auditory thalamocortical system show that cortical excitatory receptive field regions can be directly inherited from thalamus, constructed from smaller inputs, and assembled by the cooperative activity of neuronal ensembles. The prevalence of functional thalamocortical connectivity is strictly governed by tonotopy, but connection strength is not. Finally, spectral and temporal modulation preferences in cortex may differ dramatically from the thalamic input. Our observations reveal a radical reconstruction of response properties from auditory thalamus to cortex, and illustrate how some properties are propagated with great fidelity while others are significantly transformed or generated intracortically.

Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex

Many response properties in primary auditory cortex (AI) are segregated spatially and organized topographically as those in primary visual cortex. Intensive study has not revealed an intrinsic, anatomical organizing principle related to an AI functional topography. We used retrograde anatomic tracing and topographic physiologic mapping of acoustic response properties to reveal long-range (≥1.5 mm) convergent intrinsic horizontal connections between AI subregions with similar bandwidth and characteristic frequency selectivity. This suggests a modular organization for processing spectral bandwidth in AI.

A spiking neuron model of cortical correlates of sensorineural hearing loss: spontaneous firing, synchrony, and tinnitus

Hearing loss due to peripheral damage is associated with cochlear hair cell damage or loss and some retrograde degeneration of auditory nerve fibers. Surviving auditory nerve fibers in the impaired region exhibit elevated and broadened frequency tuning, and the cochleotopic representation of broadband stimuli such as speech is distorted. In impaired cortical regions, increased tuning to frequencies near the edge of the hearing loss coupled with increased spontaneous and synchronous firing is observed. Tinnitus, an auditory percept in the absence of sensory input, may arise under these circumstances as a result of plastic reorganization in the auditory cortex. We present a spiking neuron model of auditory cortex that captures several key features of cortical organization. A key assumption in the model is that in response to reduced afferent excitatory input in the damaged region, a compensatory change in the connection strengths of lateral excitatory and inhibitory connections occurs. These changes allow the model to capture some of the cortical correlates of sensorineural hearing loss, including changes in spontaneous firing and synchrony; these phenomena may explain central tinnitus. This model may also be useful for evaluating procedures designed to segregate synchronous activity underlying tinnitus and for evaluating adaptive hearing devices that compensate for selective hearing loss.

The acoustical cues to sound location in the rat: Measurements of directional transfer functions

The acoustical cues for sound location are generated by spatial- and frequency-dependent filtering of propagating sound waves by the head and external ears. Although rats have been a common model system for anatomy, physiology, and psychophysics of localization, there have been few studies of the acoustical cues available to rats. Here, directional transfer functions (DTFs), the directional components of the head-related transfer functions, were measured in six adult rats. The cues to location were computed from the DTFs. In the frontal hemisphere, spectral notches were present for frequencies from approximately 16 to 30 kHz; in general, the frequency corresponding to the notch increased with increases in source elevation and in azimuth toward the ipsilateral ear. The maximum high-frequency envelope-based interaural time differences (ITDs) were 130 mus, whereas low-frequency (<3.5 kHz) fine-structure ITDs were 160 mus; both types of ITDs were larger than predicted from spherical head models. Interaural level differences (ILDs) strongly depended on location and frequency. Maximum ILDs were <10 dB for frequencies <8 kHz and were as large as 20-40 dB for frequencies >20 kHz. Removal of the pinna eliminated the spectral notches, reduced the acoustic gain and ILDs, altered the acoustical axis, and reduced the ITDs.

Thalamic label patterns suggest primary and ventral auditory fields are distinct core regions

A hierarchical scheme proposed by Kaas and colleagues suggests that primate auditory cortex can be divided into core and belt regions based on anatomic connections with thalamus and distinctions among response properties. According to their model, core auditory cortex receives predominantly unimodal sensory input from the ventral nucleus of the medial geniculate body (MGBv); whereas belt cortex receives predominantly cross‐modal sensory input from nuclei outside the MGBv. We previously characterized distinct response properties in rat primary (A1) versus ventral auditory field (VAF) cortex; however, it has been unclear whether VAF should be categorized as a core or belt auditory cortex. The current study employed high‐resolution functional imaging to map intrinsic metabolic responses to tones and to guide retrograde tracer injections into A1 and VAF. The size and density of retrogradely labeled somas in the medial geniculate body (MGB) were examined as a function of their position along the caudal‐to‐rostral axis, subdivision of origin, and cortical projection target. A1 and VAF projecting neurons were found in the same subdivisions of the MGB but in rostral and caudal parts, respectively. Less than 3% of the cells projected to both regions. VAF projecting neurons were smaller than A1 projecting neurons located in dorsal (MGBd) and suprageniculate (SG) nuclei. Thus, soma size varied with both caudal‐rostral position and cortical target. Finally, the majority (>70%) of A1 and VAF projecting neurons were located in MGBv. These MGB connection profiles suggest that rat auditory cortex, like primate auditory cortex, is made up of multiple distinct core regions. J. Comp. Neurol. 518:1630–1646, 2010.

Spectral and Temporal Modulation Tradeoff in the Inferior Colliculus

The cochlea encodes sounds through frequency-selective channels that exhibit low-pass modulation sensitivity. Unlike the cochlea, neurons in the auditory midbrain are tuned for spectral and temporal modulations found in natural sounds, yet the role of this transformation is not known. We report a distinct tradeoff in modulation sensitivity and tuning that is topographically ordered within the central nucleus of the inferior colliculus (CNIC). Spectrotemporal receptive fields (STRFs) were obtained with 16-channel electrodes inserted orthogonal to the isofrequency lamina. Surprisingly, temporal and spectral characteristics exhibited an opposing relationship along the tonotopic axis. For low best frequencies (BFs), units were selective for fast temporal and broad spectral modulations. A systematic progression was observed toward slower temporal and finer spectral modulation sensitivity at high BF. This tradeoff was strongly reflected in the arrangement of excitation and inhibition and, consequently, in the modulation tuning characteristics. Comparisons with auditory nerve fibers show that these trends oppose the pattern imposed by the peripheral filters. These results suggest that spectrotemporal preferences are reordered within the tonotopic axis of the CNIC. This topographic organization has profound implications for the coding of spectrotemporal features in natural sounds and could underlie a number of perceptual phenomena.

Representation of spectrotemporal sound information in the ascending auditory pathway

Abstract.The representation of sound information in the central nervous system relies on the analysis of time-varying features in communication and other environmental sounds. How are auditory physiologists and theoreticians to choose an appropriate method for characterizing spectral and temporal acoustic feature representations in single neurons and neural populations? A brief survey of currently available scientific methods and their potential usefulness is given, with a focus on the strengths and weaknesses of using noise analysis techniques for approximating spectrotemporal response fields (STRFs). Noise analysis has been used to foster several conceptual advances in describing neural acoustic feature representation in a variety of species and auditory nuclei. STRFs have been used to quantitatively assess spectral and temporal transformations across mutually connected auditory nuclei, to identify neuronal interactions between spectral and temporal sound dimensions, and to compare linear vs. nonlinear response properties through state-dependent comparisons. We propose that noise analysis techniques used in combination with novel stimulus paradigms and parametric experiment designs will provide powerful means of exploring acoustic feature representations in the central nervous system.

The Contribution of Spike Threshold to Acoustic Feature Selectivity, Spike Information Content, and Information Throughput

Hypotheses of sensory coding range from the notion of nonlinear “feature detectors” to linear rate coding strategies. Here, we report that auditory neurons exhibit a novel trade-off in the relationship between sound selectivity and the information that can be communicated to a postsynaptic cell. Recordings from the cat inferior colliculus show that neurons with the lowest spike rates reliably signal the occurrence of stereotyped stimulus features, whereas those with high response rates exhibit lower selectivity. The highest information conveyed by individual action potentials comes from neurons with low spike rate and high selectivity. Surprisingly, spike information is inversely related to spike rates, following a trend similar to that of feature selectivity. Information per time interval, however, was proportional to measured spike rates. A neuronal model based on the spike threshold of the synaptic drive accurately accounts for this trade-off: higher thresholds enhance the spiking fidelity at the expense of limiting the total communicated information. Such a constraint on the specificity and throughput creates a continuum in the neural code with two extreme forms of information transfer that likely serve complementary roles in the representation of the auditory environment.

Construction and Representation of Visual Space in the Inferior Parietal Lobule

In human subjects, neurological case histories have provided details of striking deficits of cognitive functions. These findings have been supplemented by comparative studies in nonhuman primates that permit invasive manipulations and measurements of brain tissue, as well as theories that provide a structure for the synthesis and distillation of such clinical and experimental results into general principles. The formation of visuospatial representations of the surrounding world has proven to be particularly amenable to this multifaceted approach. Although far from being completely understood, substantial progress has been made in the past 20 years in the analysis of this cognitive process. One patient, suffering from profound hemi-inattention has: lost her idea of ‘left,’ both with regard to the world and her own body. Sometimes (when eating) she complains that her portions are too small, but this is because she eats only from the right half of the plate—it does not occur to her that it has a left half as well. Sometimes, she will put on lipstick, and make tip the right half of her face, leaving the left half completely neglected: It is almost impossible to treat these things, because her attention cannot be drawn to them, and she has no conception that they are wrong. She knows it intellectually, and can understand, and laugh; but it is impossible for her to know it directly. (Sacks, 1985) This particular type of spatial and attentional deficit arises from damage to associational cortical regions which were initially defined on the basis of late myelination during development (Flechsig, 1876). This patient does not have a hemianopia (half-vision field blindness), for her vision is normal. But her cognitive disassociations are in a sense more profound than blunt dissections of primary sensory or motor function. Removal of primary sensory or motor cortex leads to devastating blindness, deafness, or paralysis. But such loss can be overcome, at least in the sensory modality, by reliance on spared sensory capabilities. However, damage to the association cortex strikes at the very core of being. The patient can see but cannot attend to half of her visual world. She cannot intellectually compensate, because her spatial intellect itself is damaged. The challenge to neuroscience is to generate mechanistic explanations, perhaps reductionist, perhaps synthetic, to account for normal cognitive deficits on this scale. These explanations might explain cognitive function in the normal individual.

Spectrotemporal sound preferences of neighboring inferior colliculus neurons: implications for local circuitry and processing

How do local circuits in the inferior colliculus (IC) process and transform spectral and temporal sound information? Using a four-tetrode array we examined the functional properties of the IC and metrics of its micro circuitry by recording neural activity from neighboring single neurons in the cat. Spectral and temporal response preferences were compared for neurons found on the same and adjacent tetrodes (ATs), as well as across distant recording sites. We found that neighboring neurons had similar preferences while neurons recorded across distant sites were less similar. Best frequency (BF) was the most correlated parameter between neighboring neurons and BF differences exhibited unique clustering at ~0.3 octave intervals, indicative of the frequency band lamina. Other spectral and temporal parameters of the receptive fields were more similar for neighboring neurons than for those at distant sites and the receptive field similarity was larger for neurons with small differences in BF. Furthermore, correlated firing was stronger for neighboring neuron pairs and increased with proximity and decreasing BF difference. Thus, although response selectivities are quite diverse in the IC, spectral, and temporal preference within a local microcircuit are functionally quite similar. This suggests a scheme where local circuits are organized into zones that are specialized for processing distinct spectrotemporal cues.