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Connections of the mesencephalic, thalamic and telencephalic auditory centers in turtles. Some structural bases for audiosomatic interrelations.

The organization of auditory projections at the mesencephalic, thalamic and telencephalic brain levels was studied utilizing the method of horseradish peroxidase (HRP) transport in two species of the turtle--Emys orbicularis and Testudo horsfieldi. It was shown that the torus semicircularis receives bilateral afferents from the brain stem auditory centers. They arise predominantly from the contralateral cochlear nuclei, the ipsilateral superior olive, the dorsal and ventral nuclei of the lateral lemniscus and from the symmetrical torus semicircularis. These connections appear to be reciprocal. After the enzyme injections correspondingly into the torus semicircularis and n. reuniens anterograde and retrograde HRP transports show that the central nucleus of the torus semicircularis projects to n. reuniens throughout its rostro-caudal extent mainly ipsilaterally. In turn, n. reuniens projects to the medioventral part of the dorsal ventricular ridge. A following common principle of the organization of the auditory system was revealed at the three brain levels explored. Auditory relay centers occupy the most medial positions at every level (n. centralis of the torus semicircularis, n. reuniens, the medioventral part of the dorsal ventricular ridge). Immediately lateral to them are somatic centers (correspondingly, n. intercollicularis, n. ventralis, the central part of the dorsal ventricular ridge). These together with the auditory centers form united functional complexes at every level. In these complexes auditory and somatic projections overlap, thus constituting a basis for the interaction between auditory and somatic afferent inputs. Mesencephalic and thalamic auditory centers were shown to receive direct somatic (cervical spinal) projections and non-direct from the underlying somatic center as well as from the adjacent somatic center at the same level (n. intercollicularis in the mesencephalon, n. ventralis in the thalamus). Somatic centers in the complexes described get no direct auditory projections. Auditory impulses however can enter them via two pathways: along neuron axons from the neighbouring auditory center reaching the adjacent somatic center and along somatic neuron dendrites which pass into the adjacent auditory center. The morphological basis for the auditory-somatic interactions primarily in the auditory center and also in the somatic center was demonstrated in Golgi-like HRP labeled and Golgi-impregnated neurons of these centers. The organization of the auditory-somatic projections at the three brain levels in turtles in to a degree comparable to the auditory system in mammals which is structured according to the core-belt principle.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Processing of complex sounds in the auditory cortex of cat, monkey, and man.

One of the fundamental features in the organization of sensory cortices which has emerged from 30 years of research in the visual system is the existence of multiple representation of the sensory world in the cerebral cortex. Compared with the visual system much less information exists about the functional specialization of multiple maps in the central auditory system. This is surprising, since an understanding of central auditory representations seems necessary for an understanding of higher auditory processing, including the perception of speech and the perception of auditory space. We have recorded single neuron activity in higher areas of auditory cortex of cats and rhesus monkeys. In cats, activity was recorded in the caudal part of the anterior ectosylvian (AE) cortex (areas AEA and AAF). More than half of the neurons were clearly tuned to the location of a sound source in azimuth and elevation. Frequency-modulated (FM) sounds elicited best responses at fast rates of modulation. By contrast, neurons in the posterior ectosylvian (PE) areas (PAF, VPAF) responded better to slow FM rates. This suggests a possible specialization for the processing of spatial attributes in the AE cortex, and a possible preference for auditory "patterns" in PE. In macaque monkeys, we explored the question of parallel processing in the higher auditory pathways by combining lesion and anatomical tracer techniques with single unit recording. Inactivation of primary auditory cortex (AI) abolished pure-tone responses in the caudomedial area (CM), but not in the rostral area (R). Injections of retrograde fluorescent tracers into R showed strong labeling of the main, ventral nucleus of the medial geniculate (MGv). Both findings suggest the existence of parallel pathways in the auditory cortex, originating at more peripheral sites and possibly specialized for the processing of auditory space vs. auditory patterns. The auditory pattern pathway in Macaque auditory cortex was further explored by using complex stimuli including Macaque-specific communication sounds. Neurons in the lateral belt areas (AL, ML, and CL) respond very selectively to bandpassed noise stimuli, to FM sounds of a certain rate and direction, as well as to certain classes of monkey calls. We are now in the process of exploring higher areas of human auditory cortex by measuring cortical activation with noninvasive functional magnetic resonance imaging (fMRI) while stimulating with complex auditory sounds.

Animals↗

Responses to auditory stimuli in macaque lateral intraparietal area. I. Effects of training.

The lateral intraparietal area (LIP) of macaques has been considered unresponsive to auditory stimulation. Recent reports, however, indicate that neurons in this area respond to auditory stimuli in the context of an auditory-saccade task. Is this difference in auditory responsiveness of LIP due to auditory-saccade training? To address this issue, LIP responses in two monkeys were recorded at two different times: before and after auditory-saccade training. Before auditory-saccade training, the animals had never been trained on any auditory task, but had been trained on visual tasks. In both sets of experiments, activity of LIP neurons was recorded while auditory and visual stimuli were presented and the animals were fixating. Before training, 172 LIP neurons were recorded. Among these, the number of cells responding to auditory stimuli did not reach significance, whereas about one-half of the cells responded to visual stimuli. An information theory analysis confirmed that no information about auditory stimulus location was available in LIP neurons in the experiments before training. After training, activity from 160 cells was recorded. These experiments showed that 12% of cells in area LIP responded to auditory stimuli, whereas the proportion of cells responding to visual stimuli remained about the same as before training. The information theory analysis confirmed that, after training, information about auditory stimulus location was available in LIP neurons. Auditory-saccade training therefore generated responsiveness to auditory stimuli de novo in LIP neurons. Thus some LIP cells become active for auditory stimuli in a passive fixation task, once the animals have learned that these stimuli are important for oculomotor behavior.

Acoustic Stimulation↗

Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals.

Based on the findings of the preceding paper, it is known that auditory and visual signals have been translated into common coordinates at the level of the superior colliculus (SC) and share a motor circuit involved in the generation of saccadic eye movements. It is not known, however, whether the translation of sensory signals into motor coordinates occurs prior to or within the SC. Nor is it known in what coordinates auditory signals observed in the SC are encoded. The present experiment tested two alternative hypotheses concerning the frame of reference of auditory signals found in the deeper layers of the SC. The hypothesis that auditory signals are encoded in head coordinates predicts that, with the head stationary, the response of auditory neurons will not be affected by variations in eye position but will be determined by the location of the sound source. The hypothesis that auditory responses encode the trajectory of the eye movement required to look to the target (motor error) predicts that the response of auditory cells will depend on both the position of the sound source and the position of the eyes in the orbit. Extracellular single-unit recordings were obtained from neurons in the SC while monkeys made delayed saccades to auditory or visual targets in a darkened room. The coordinates of auditory signals were studied by plotting auditory receptive fields while the animal fixated one of three targets placed 24 degrees apart along the horizontal plane. For 99 of 121 SC cells, the spatial location of the auditory receptive field was significantly altered by the position of the eyes in the orbit. In contrast, the responses of five sound-sensitive cells isolated in the inferior colliculus were not affected by variations in eye position. The possibility that systematic variations in the position of the pinnae associated with different fixation positions could account for these findings was controlled for by plotting auditory receptive fields while the pinnae were mechanically restrained. Under these conditions, the position of the eyes in the orbit still had a significant effect on the responsiveness of collicular neurons to auditory stimuli. The average magnitude of the shift of the auditory receptive field with changes in eye position (12.9 degrees) did not correspond to the magnitude of the shift in eye position (24 degrees). Alternative explanations for this finding were considered. One possibility is that, within the SC, there is a gradual transition from auditory signals in head coordinates to signals in motor error coordinates.(ABSTRACT TRUNCATED AT 400 WORDS)

Acoustic Stimulation↗

"Auditory neuropathy": physiologic and pathologic evidence calls for more diagnostic specificity.

The term "auditory neuropathy" is being used in a rapidly increasing number of papers in the audiology/otolaryngology literature for a variety of individuals (mostly children) who fulfill the following criteria: (1) understanding of speech worse than predicted from the degree of hearing loss on their behavioral audiograms; (2) recordable otoacoustic emissions and/or cochlear microphonic; together with (3) absent or atypical auditory brain stem responses. Because of the general lack of anatomic foundation for the label "auditory neuropathy" as currently used, we review the anatomy of the auditory pathway, the definition of neuropathy and its demyelinating, axonal, and mixed variants. We submit that the diagnostic term "auditory neuropathy" is anatomically inappropriate unless patients have documented evidence for selective involvement of either the spiral ganglion cells or their axons, or of the 8th nerve as a whole. In view of biologic differences between peripheral nerves and white matter tracts in the brain, the term "auditory neuropathy" is inappropriate for pathologies affecting the central auditory pathway in the brainstem and brain selectively. Published reports of patients with "auditory neuropathy" indicate that they are extremely heterogeneous in underlying medical diagnosis, age, severity, test results, and that only a small number have undergone the detailed investigations that would enable a more precise diagnosis of the locus of their pathologies. The electrophysiology of peripheral neuropathies and the deficits expected with pathologies affecting the hair cells, spiral ganglion cells and their axons (auditory neuropathy sensu stricto), and brain stem relays are reviewed. In order to serve patients adequately, including potential candidates for cochlear implants, and to increase knowledge of auditory pathologies, we make a plea for more comprehensive evaluation of patients who fulfill the currently used audiologic criteria for "auditory neuropathy" in an effort to pinpoint the site of their pathologies. We suggest that the term auditory neuropathy be limited to cases in which the locus of pathology is limited to the spiral ganglion cells, their processes, or the 8th nerve, and that the term neural hearing loss be considered for pathologies that affect all higher levels of the auditory pathway, from the brainstem to the auditory cortex.

Audiology↗