Space-specific Neurons Research Articles

Binaural Cross-Correlation Predicts the Responses of Neurons in the Owl’s Auditory Space Map under Conditions Simulating Summing Localization

Summing localization describes the perceptions of human listeners to two identical sounds from different locations presented with delays of 0-1 msec. Usually a single source is perceived to be located between the two actual source locations, biased toward the earlier source. We studied neuronal responses within the space map of the barn owl to sounds presented with this same paradigm. The owl's primary cue for localization along the azimuth, interaural time difference (ITD), is based on a cross-correlation-like treatment of the signals arriving at each ear. The output of this cross-correlation is displayed as neural activity across the auditory space map in the external nucleus of the owl's inferior colliculus. Because the ear input signals reflect the physical summing of the signals generated by each speaker, we first recorded the sounds at each ear and computed their cross-correlations at various interstimulus delays. The resulting binaural cross-correlation surface strongly resembles the pattern of activity across the space map inferred from recordings of single space-specific neurons. Four peaks are observed in the cross-correlation surface for any nonzero delay. One peak occurs at the correlation delay equal to the ITD of each speaker. Two additional peaks reflect "phantom sources" occurring at correlation delays that match the signal of the left speaker in one ear with the signal of the right speaker in the other ear. At zero delay, the two phantom peaks coincide. The surface features are complicated further by the interactions of the various correlation peaks.

Responses to simulated echoes by neurons in the barn owl's auditory space map.

The natural acoustical environment contains many reflective surfaces that give rise to echoes, complicating the task of sound localization and identification. The barn owl (Tyto alba), as a nocturnal predator, relies heavily on its auditory system for tracking and capturing prey in this highly echoic environment. The external nucleus of the owl's inferior colliculus (ICx) contains a retina-like map of space composed of "space-specific" auditory neurons that have spatially limited receptive fields. We recorded extracellularly from individual space-specific neurons in an attempt to understand the pattern of activity across the ICx in response to a brief direct sound and a simulated echo. Space-specific neurons responded strongly to the direct sound, but their response to a simulated echo was suppressed, typically, if the echo arrived within 5 ms or less of the direct sound. Thus we expect there to be little or no representation within the ICx of echoes arriving within such short delays. Behavioral tests using the owl's natural tendency to turn their head toward a sound source suggested that owls, like their space-specific neurons, similarly localize only the first of two brief sounds. Naive, untrained owls were presented with a pair of sounds in rapid succession from two horizontally-separated speakers. With interstimulus delays of less than 10 ms, the owl consistently turned its head toward the leading speaker. Longer delays elicited head turns to either speaker with approximately equal frequency and in some cases to both speakers sequentially.

Construction of an auditory space map.

The computation of ITD begins with preservation of the phase angle of spectral components by eighth-nerve fibers and by cells of the nucleus magnocellularis. At the level of the nucleus laminaris, the difference in phase angle of corresponding spectral components in the left and right ears is extracted. At the next level, the central nucleus, neurons are consolidated into tonotopic ensembles in which preferred delta phi and frequency covary, so that only a single ITD coactivates all constituent neurons. Neurons of such ensembles project convergently on space-specific neurons, endowing the space-specific neuron with a selectivity for ITD and, therefore, a selectivity for azimuth. Ensembles representing ITDs corresponding to ipsilateral and contralateral auditory hemi-fields are found in the core and lateral shell of the central nucleus, respectively. The lateral shell receives its representation of the contralateral hemi-field from the opposite central nucleus core. The central nucleus core is innervated by the contralateral nucleus laminaris, which contains a representation of contralateral space. The projection from the lateral shell to the ipsilateral external nucleus forms a map of contralateral space in the external nucleus.

Representation of interaural 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.

Time and intensity cues are processed independently in the auditory system of the owl

Space-specific neurons, found in the barn owl's inferior colliculus, respond selectively to a narrow range of interaural time and intensity differences. We show that injecting a local anesthetic into one cochlear nucleus, nucleus magnocellularis, alters the space-specific cell's selectivity for interaural time difference, leaving its selectivity for interaural intensity difference intact. Anesthetizing the other cochlear nucleus, nucleus angularis, has the converse effects. We show also that the space-specific neuron's selectivity for one interaural cue is the same for all effective values of the other cue. We conclude that time and intensity cues are processed in separate neural channels of the barn owl's auditory system and that the two cues operate independently.

Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization.

Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization.

Some neural mechanisms in the inferior colliculus of the cat which may be relevant to localization of a sound source.

Some neural mechanisms in the inferior colliculus of the cat which may be relevant to localization of a sound source.

Tonal discrimination after ablation of auditory cortex.

ArticlesTONAL DISCRIMINATION AFTER ABLATION OF AUDITORY CORTEXIrving T. Diamond, Jay M. Goldberg, and William D. NeffIrving T. Diamond, Jay M. Goldberg, and William D. NeffPublished Online:01 Mar 1962https://doi.org/10.1152/jn.1962.25.2.223MoreSectionsPDF (2 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformationCited ByComparison of Midbrain and Thalamic Space-Specific Neurons in Barn OwlsMaría Lucía Pérez, and José Luis Peña1 February 2006 | Journal of Neurophysiology, Vol. 95, No. 2Sound sequence discrimination learning is dependent on cholinergic inputs to the rat auditory cortexNeuroscience Research, Vol. 50, No. 1Processing of Sound Sequences in Macaque Auditory Cortex: Response EnhancementMichael Brosch, Andreas Schulz, and Henning Scheich1 September 1999 | Journal of Neurophysiology, Vol. 82, No. 3Time Course of Forward Masking Tuning Curves in Cat Primary Auditory CortexMichael Brosch, and Christoph E. Schreiner1 February 1997 | Journal of Neurophysiology, Vol. 77, No. 2Auditory perception of temporal and spectral events in patients with focal left and right cerebral lesionsBrain and Language, Vol. 39, No. 4Psychic ageusia in rats lacking gustatory neocortexExperimental Neurology, Vol. 72, No. 3Sequential auditory and visual discriminations after temporal lobe ablation in monkeysPhysiology & Behavior, Vol. 24, No. 6Duration Discrimination in the Rat after Early Auditory Restriction2 November 2016 | Perceptual and Motor Skills, Vol. 25, No. 1 More from this issue > Volume 25Issue 2March 1962Pages 223-235 https://doi.org/10.1152/jn.1962.25.2.223PubMed13886108History Published online 1 March 1962 Published in print 1 March 1962 Metrics

Ablation of temporal cortex and discrimination of auditory patterns.

ArticlesABLATION OF TEMPORAL CORTEX AND DISCRIMINATION OF AUDITORY PATTERNSIrving T. Diamond, and W. D. NeffIrving T. Diamond, and W. D. NeffPublished Online:01 May 1957https://doi.org/10.1152/jn.1957.20.3.300MoreSectionsPDF (2 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformation Cited ByEarly Stages of Melody Processing: Stimulus-Sequence and Task-Dependent Neuronal Activity in Monkey Auditory Cortical Fields A1 and RPingbo Yin, Mortimer Mishkin, Mitchell Sutter, and Jonathan B. Fritz1 December 2008 | Journal of Neurophysiology, Vol. 100, No. 6Single-Neuron Responses to Rapidly Presented Temporal Sequences in the Primary Auditory Cortex of the Awake Macaque MonkeyM. L. Phan, and G. H. Recanzone1 February 2007 | Journal of Neurophysiology, Vol. 97, No. 2Comparison of Midbrain and Thalamic Space-Specific Neurons in Barn OwlsMaría Lucía Pérez, and José Luis Peña1 February 2006 | Journal of Neurophysiology, Vol. 95, No. 2Sound sequence discrimination learning is dependent on cholinergic inputs to the rat auditory cortexNeuroscience Research, Vol. 50, No. 1Processing of Sound Sequences in Macaque Auditory Cortex: Response EnhancementMichael Brosch, Andreas Schulz, and Henning Scheich1 September 1999 | Journal of Neurophysiology, Vol. 82, No. 3Time Course of Forward Masking Tuning Curves in Cat Primary Auditory CortexMichael Brosch, and Christoph E. Schreiner1 February 1997 | Journal of Neurophysiology, Vol. 77, No. 2Neural coding of speech sound in the telencephalic auditory area of the mynah birdJournal of Comparative Physiology A, Vol. 169, No. 2Auditory perception of temporal and spectral events in patients with focal left and right cerebral lesionsBrain and Language, Vol. 39, No. 4Central action of endogenous sugar acid (2-buten-4-olide): Comparison with local anesthesia in hypothalamusBrain Research Bulletin, Vol. 24, No. 6Characteristics of rat lateral hypothalamic neuron responses to smell and taste in emotional behaviorBrain Research, Vol. 491, No. 1Neuromagnetic responses of human auditory cortex to interruptions in a steady rhythmNeuroscience Letters, Vol. 99, No. 1-2Responses of single auditory cortical neurons to tone sequencesBrain Research, Vol. 481, No. 1Representation of amplitude modulation in the auditory cortex of the cat. II. Comparison between cortical fieldsHearing Research, Vol. 32, No. 1Age-related changes in auditory temporal perceptionJournal of Experimental Child Psychology, Vol. 44, No. 3Representation of amplitude modulation in the auditory cortex of the cat. I. 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Intrahemispheric cortical afferentsBrain Research, Vol. 132, No. 2The Brain and Hearing: Auditory Discriminations Affected by Brain Lesions29 June 2016 | Annals of Otology, Rhinology & Laryngology, Vol. 86, No. 4Effect of auditory neocortex ablation on identification of click rates in catsBrain Research, Vol. 116, No. 1A microelectrode study of amygdaloid afferents: Temporal neocortical inputsBrain Research, Vol. 105, No. 3Some variables in auditory pattern discrimination learningNeuropsychologia, Vol. 14, No. 2Auditory and visual discrimination following lesions of the anterior supratemporal plane in monkeysNeuropsychologia, Vol. 14, No. 2Etude psychoacoustique d'un cas de “surdite corticale”Neuropsychologia, Vol. 13, No. 2Polysensory cortical lesions and auditory temporal pattern discriminations in the catBrain Research, Vol. 80, No. 2Insular-temporal lesions and vibrotactile temporal pattern discrimination in catsPhysiology & Behavior, Vol. 12, No. 2The effects of insular and temporal lesions in cats on two types of auditory pattern discriminationBrain Research, Vol. 62, No. 1Responses of single units in the primary auditory cortex of the cat to tones and to tone pairsBrain Research, Vol. 42, No. 2Auditory cortical lesions and visual pattern discrimination in catBrain Research, Vol. 39, No. 2Thalam-Cortical Organization of the Auditory System in the CatProceedings of the Japan Academy, Vol. 48, No. 8Neural structures mediating differential sound intensity discrimination in the catBrain Research, Vol. 27, No. 2Effects of ablations of temporal cortex upon speech sound discrimination in the monkeyExperimental Neurology, Vol. 24, No. 4Duration Discrimination in the Rat after Early Auditory Restriction2 November 2016 | Perceptual and Motor Skills, Vol. 25, No. 1Temporal conditioning of the arousal responsePhysiology & Behavior, Vol. 2, No. 1Auditory organization of the inferior colliculi in the catExperimental Neurology, Vol. 6, No. 6 More from this issue > Volume 20Issue 3May 1957Pages 300-315 https://doi.org/10.1152/jn.1957.20.3.300PubMed13429392History Published online 1 May 1957 Published in print 1 May 1957 Metrics