scholarly journals Comparison of Midbrain and Thalamic Space-Specific Neurons in Barn Owls

2006 ◽  
Vol 95 (2) ◽  
pp. 783-790 ◽  
Author(s):  
María Lucía Pérez ◽  
José Luis Peña

Spatial receptive fields of neurons in the auditory pathway of the barn owl result from the sensitivity to combinations of interaural time (ITD) and level differences across stimulus frequency. Both the forebrain and tectum of the owl contain such neurons. The neural pathways, which lead to the forebrain and tectal representations of auditory space, separate before the midbrain map of auditory space is synthesized. The first nuclei that belong exclusively to either the forebrain or the tectal pathways are the nucleus ovoidalis (Ov) and the external nucleus of the inferior colliculus (ICx), respectively. Both receive projections from the lateral shell subdivision of the inferior colliculus but are not interconnected. Previous studies indicate that the owl's tectal representation of auditory space is different from those found in the owl's forebrain and the mammalian brain. We addressed the question of whether the computation of spatial cues in both pathways is the same by comparing the ITD tuning of Ov and ICx neurons. Unlike in ICx, the relationship between frequency and ITD tuning had not been studied in single Ov units. In contrast to the conspicuous frequency independent ITD tuning of space-specific neurons of ICx, ITD selectivity varied with frequency in Ov. We also observed that the spatially tuned neurons of Ov respond to lower frequencies and are more broadly tuned to ITD than in ICx. Thus there are differences in the integration of frequency and ITD in the two sound-localization pathways. Thalamic neurons integrate spatial information not only within a broader frequency band but also across ITD channels.

2006 ◽  
Vol 96 (2) ◽  
pp. 813-825 ◽  
Author(s):  
Yoram Gutfreund ◽  
Eric I. Knudsen

Auditory neurons in the owl’s external nucleus of the inferior colliculus (ICX) integrate information across frequency channels to create a map of auditory space. This study describes a powerful, sound-driven adaptation of unit responsiveness in the ICX and explores the implications of this adaptation for sensory processing. Adaptation in the ICX was analyzed by presenting lightly anesthetized owls with sequential pairs of dichotic noise bursts. Adaptation occurred in response even to weak, threshold-level sounds and remained strong for more than 100 ms after stimulus offset. Stimulation by one range of sound frequencies caused adaptation that generalized across the entire broad range of frequencies to which these units responded. Identical stimuli were used to test adaptation in the lateral shell of the central nucleus of the inferior colliculus (ICCls), which provides input directly to the ICX. Compared with ICX adaptation, adaptation in the ICCls was substantially weaker, shorter lasting, and far more frequency specific, suggesting that part of the adaptation observed in the ICX was attributable to processes resident to the ICX. The sharp tuning of ICX neurons to space, along with their broad tuning to frequency, allows ICX adaptation to preserve a representation of stimulus location, regardless of the frequency content of the sound. The ICX is known to be a site of visually guided auditory map plasticity. ICX adaptation could play a role in this cross-modal plasticity by providing a short-term memory of the representation of auditory localization cues that could be compared with later-arriving, visual–spatial information from bimodal stimuli.


2018 ◽  
Vol 119 (3) ◽  
pp. 1235-1247 ◽  
Author(s):  
Roland Ferger ◽  
Kerstin Pawlowsky ◽  
Martin Singheiser ◽  
Hermann Wagner

Response adaptation is the change of the firing rate of neurons induced by a preceding stimulus. It can be found in many sensory systems and throughout the auditory pathway. We investigated response adaptation in the external nucleus of the inferior colliculus (ICX) of barn owls ( Tyto furcata), a nocturnal bird of prey and specialist in sound localization. Individual neurons in the ICX represent locations in auditory space by maximally responding to combinations of interaural time and level differences (ITD and ILD). Neuronal responses were recorded extracellularly under ketamine-diazepam anesthesia. Response adaptation was observed in three double stimulation paradigms. In two paradigms, the same binaural parameters for both stimuli were chosen. A variation of the level of the second stimulus yielded a level increase sufficient to compensate for adaptation around 5 dB. Introducing a silent interstimulus interval (ISI) resulted in recovery from adaptation. The time course of recovery was followed by varying the ISI, and full recovery was found after an ISI of 50 ms. In a third paradigm, the ITD of the second stimulus was varied to investigate the representation of ITD under adaptive conditions. We found that adaptation led to an increased precision and improved selectivity while the best ITD was stable. These changes of representation remained for longer ISIs than were needed to recover from response adaptation at the best ITD. Stimuli with non-best ITDs could also induce similar adaptive effects if the neurons responded to these ITDs. NEW & NOTEWORTHY We demonstrate and characterize response adaptation in neurons of the auditory space map in the barn owl’s midbrain with acoustic double-stimulation paradigms. An increase of the second level by 5 dB compensated for the observed adaptive effect. Recovery from adaptation was faster than in upstream nuclei of the auditory pathway. Our results also show that response adaptation might improve precision and selectivity in the representation of interaural time difference.


2005 ◽  
Vol 94 (4) ◽  
pp. 2331-2352 ◽  
Author(s):  
O'Dhaniel A. Mullette-Gillman ◽  
Yale E. Cohen ◽  
Jennifer M. Groh

The integration of visual and auditory events is thought to require a joint representation of visual and auditory space in a common reference frame. We investigated the coding of visual and auditory space in the lateral and medial intraparietal areas (LIP, MIP) as a candidate for such a representation. We recorded the activity of 275 neurons in LIP and MIP of two monkeys while they performed saccades to a row of visual and auditory targets from three different eye positions. We found 45% of these neurons to be modulated by the locations of visual targets, 19% by auditory targets, and 9% by both visual and auditory targets. The reference frame for both visual and auditory receptive fields ranged along a continuum between eye- and head-centered reference frames with ∼10% of auditory and 33% of visual neurons having receptive fields that were more consistent with an eye- than a head-centered frame of reference and 23 and 18% having receptive fields that were more consistent with a head- than an eye-centered frame of reference, leaving a large fraction of both visual and auditory response patterns inconsistent with both head- and eye-centered reference frames. The results were similar to the reference frame we have previously found for auditory stimuli in the inferior colliculus and core auditory cortex. The correspondence between the visual and auditory receptive fields of individual neurons was weak. Nevertheless, the visual and auditory responses were sufficiently well correlated that a simple one-layer network constructed to calculate target location from the activity of the neurons in our sample performed successfully for auditory targets even though the weights were fit based only on the visual responses. We interpret these results as suggesting that although the representations of space in areas LIP and MIP are not easily described within the conventional conceptual framework of reference frames, they nevertheless process visual and auditory spatial information in a similar fashion.


2010 ◽  
Vol 90 (3) ◽  
pp. 983-1012 ◽  
Author(s):  
Benedikt Grothe ◽  
Michael Pecka ◽  
David McAlpine

The ability to determine the location of a sound source is fundamental to hearing. However, auditory space is not represented in any systematic manner on the basilar membrane of the cochlea, the sensory surface of the receptor organ for hearing. Understanding the means by which sensitivity to spatial cues is computed in central neurons can therefore contribute to our understanding of the basic nature of complex neural representations. We review recent evidence concerning the nature of the neural representation of auditory space in the mammalian brain and elaborate on recent advances in the understanding of mammalian subcortical processing of auditory spatial cues that challenge the “textbook” version of sound localization, in particular brain mechanisms contributing to binaural hearing.


1998 ◽  
Vol 79 (2) ◽  
pp. 891-902 ◽  
Author(s):  
Yale E. Cohen ◽  
Greg L. Miller ◽  
Eric I. Knudsen

Cohen, Yale E., Greg L. Miller, and Eric I. Knudsen. Forebrain pathway for auditory space processing in the barn owl. J. Neurophysiol. 79: 891–902, 1998. The forebrain plays an important role in many aspects of sound localization behavior. Yet, the forebrain pathway that processes auditory spatial information is not known for any species. Using standard anatomic labeling techniques, we used a “top-down” approach to trace the flow of auditory spatial information from an output area of the forebrain sound localization pathway (the auditory archistriatum, AAr), back through the forebrain, and into the auditory midbrain. Previous work has demonstrated that AAr units are specialized for auditory space processing. The results presented here show that the AAr receives afferent input from Field L both directly and indirectly via the caudolateral neostriatum. Afferent input to Field L originates mainly in the auditory thalamus, nucleus ovoidalis, which, in turn, receives input from the central nucleus of the inferior colliculus. In addition, we confirmed previously reported projections of the AAr to the basal ganglia, the external nucleus of the inferior colliculus (ICX), the deep layers of the optic tectum, and various brain stem nuclei. A series of inactivation experiments demonstrated that the sharp tuning of AAr sites for binaural spatial cues depends on Field L input but not on input from the auditory space map in the midbrain ICX: pharmacological inactivation of Field L eliminated completelyauditory responses in the AAr, whereas bilateral ablation of the midbrain ICX had no appreciable effect on AAr responses. We conclude, therefore, that the forebrain sound localization pathway can process auditory spatial information independently of the midbrain localization pathway.


1998 ◽  
Vol 79 (2) ◽  
pp. 879-890 ◽  
Author(s):  
Yale E. Cohen ◽  
Eric I. Knudsen

Cohen, Yale E. and Eric I. Knudsen. Representation of binaural spatial cues in Field L of the barn owl forebrain. J. Neurophysiol. 79: 879–890, 1998. This study examined the representation of spatial information in the barn owl Field L, the first telencephalic processing stage of the classical auditory pathway. Field L units were recorded extracellularly, and their responses to dichotically presented interaural time differences (ITD) and interaural level differences (ILD) were tested. We observed a variety of tuning profiles in Field L. Some sites were not sensitive to ITD or ILD. Other sites, especially those in the high-frequency region, were highly selective for values of ITD and ILD. These sites had multipeaked (commonly called “phase ambiguous”) ITD tuning profiles and were tuned for a single value of ILD. The tuning properties of these sites are similar to those seen in the lateral shell of the central nucleus of the inferior colliculus. Although the tuning properties of Field L sites were similar to those observed in the inferior colliculus, the functional organization of this spatial information was fundamentally different. Whereas in the inferior colliculus spatial information is organized into global topographics maps, in Field L spatial information is organized into local clusters, with sites having similar binaural tuning properties grouped together. The representation of binaural cues in Field L suggests that it is involved in auditory space processing but at a lower level of information processing than the auditory archistriatum, a forebrain area that is specialized for processing spatial information, and that the levels of information processing in the forebrain space processing pathway are remarkably similar to those in the well-known midbrain space processing pathway.


2014 ◽  
Vol 111 (10) ◽  
pp. 2047-2060 ◽  
Author(s):  
James A. Morrison ◽  
Faranak Farzan ◽  
Thane Fremouw ◽  
Riziq Sayegh ◽  
Ellen Covey ◽  
...  

Neurons throughout the mammalian central auditory pathway respond selectively to stimulus frequency and amplitude, and some are also selective for stimulus duration. First found in the auditory midbrain or inferior colliculus (IC), these duration-tuned neurons (DTNs) provide a potential neural mechanism for encoding temporal features of sound. In this study, we investigated how having an additional neural response filter, one selective to the duration of an auditory stimulus, influences frequency tuning and neural organization by recording single-unit responses and measuring the dorsal-ventral position and spectral-temporal tuning properties of auditory DTNs from the IC of the awake big brown bat ( Eptesicus fuscus). Like other IC neurons, DTNs were tonotopically organized and had either V-shaped, U-shaped, or O-shaped frequency tuning curves (excitatory frequency response areas). We hypothesized there would be an interaction between frequency and duration tuning in DTNs, as electrical engineering theory for resonant filters dictates a trade-off in spectral-temporal resolution: sharp tuning in the frequency domain results in poorer resolution in the time domain and vice versa. While the IC is a more complex signal analyzer than an electrical filter, a similar operational trade-off could exist in the responses of DTNs. Our data revealed two patterns of spectro-temporal sensitivity and spatial organization within the IC: DTNs with sharp frequency tuning and broad duration tuning were located in the dorsal IC, whereas cells with wide spectral tuning and narrow temporal tuning were found in the ventral IC.


1987 ◽  
Vol 57 (4) ◽  
pp. 1130-1147 ◽  
Author(s):  
M. N. Semple ◽  
L. M. Kitzes

The central auditory system could encode information about the location of a high-frequency sound source by comparing the sound pressure levels at the ears. Two potential computations are the interaural intensity difference (IID) and the average binaural intensity (ABI). In this study of the central nucleus of the inferior colliculus (ICC) of the anesthetized gerbil, we demonstrate that responses of 85% of the 97 single units in our sample were jointly influenced by IID and ABI. For a given ABI, discharge rate of most units is a sigmoidal function of IID, and peak rates occur at IIDs favoring the contralateral ear. Most commonly, successive increments of ABI cause successive shifts of the IID functions toward IIDs favoring the ipsilateral ear. Neurons displaying this behavior include many that would conventionally be classified EI (receiving predominantly excitatory input arising from one ear and inhibitory input from the other), many that would be classified EE (receiving predominantly excitatory input arising from each ear), and all that are responsive only to contralateral stimulation. The IID sensitivity of a very few EI neurons is unaffected by ABI, except near threshold. Such units could provide directional information that is independent of source intensity. A few EE neurons are very sensitive to ABI, but are minimally sensitive to IID. Nevertheless, our data indicate that responses of most EE units in ICC are strongly dominated by excitation of contralateral origin. For some units, discharge rate is nonmonotonically related to IID and is maximal when the stimuli at the two ears are of comparable sound pressure. This preference for zero IID is common for all binaural levels. Many EI neurons respond nonmonotonically to ABI. Discharge rates are greater for IIDs representative of contralateral space and are maximal at a single best ABI. For a subset of these neurons, the influence arising from the ipsilateral ear is comprised of a mixture of excitation and inhibition. As a consequence, discharge rates are nonmonotonically related not only to ABI but also to IID. This dual nonmonotonicity creates a clear focus of peak response at a particular ABI/IID combination. Because of their mixed monaural influences, such units would be ascribed to different classes of the conventional (EE/EI) binaural classification scheme depending on the binaural level presented. Several response classes were identified in this study, and each might contribute differently to the encoding of spatial information.(ABSTRACT TRUNCATED AT 400 WORDS)


1988 ◽  
Vol 60 (6) ◽  
pp. 1799-1822 ◽  
Author(s):  
G. Langner ◽  
C. E. Schreiner

1. Temporal properties of single- and multiple-unit responses were investigated in the inferior colliculus (IC) of the barbiturate-anesthetized cat. Approximately 95% of recording sites were located in the central nucleus of the inferior colliculus (ICC). Responses to contralateral stimulation with tone bursts and amplitude-modulated tones (100% sinusoidal modulation) were recorded. Five response parameters were determined for neurons at each location: 1) characteristic frequency (CF); 2) onset latency of responses to CF-tones 60 dB above threshold; 3) Q10 dB (CF divided by bandwidth of tuning curve 10 dB above threshold); 4) best modulation frequency for firing rate (rBMF or BMF; amplitude modulation frequency that elicited the highest firing rate); and 5) best modulation frequency for synchronization (sBMF; amplitude modulation frequency that elicited the highest degree of phase-locking to the modulation frequency). 2. Response characteristics for single units and multiple units corresponded closely. A BMF was obtained at almost all recording sites. For units with a similar CF, a range of BMFs was observed. The upper limit of BMF increased approximately proportional to CF/4 up to BMFs as high as 1 kHz. The lower limit of encountered BMFs for a given CF also increased slightly with CF. BMF ranges for single-unit and multiple-unit responses were similar. Twenty-three percent of the responses revealed rBMFs between 10 and 30 Hz, 51% between 30 and 100 Hz, 18% between 100 and 300 Hz, and 8% between 300 and 1000 Hz. 3. For single units with modulation transfer functions of bandpass characteristics, BMFs determined for firing rate and synchronization were similar (r2 = 0.95). 4. Onset latencies for responses to CF tones 60 dB above threshold varied between 4 and 120 ms. Ninety percent of the onset latencies were between 5 and 18 ms. A range of onset latencies was recorded for different neurons with any given CF. The onset response latency of a given unit or unit cluster was significantly correlated with the period of the BMF and the period of the CF (P less than 0.05). 5."Intrinsic oscillations" of short duration, i.e., regularly timed discharges of units in response to stimuli without a corresponding temporal structure, were frequently observed in the ICC. Oscillation intervals were commonly found to be integer multiples of 0.4 ms. Changes of stimulus frequency or intensity had only minor influences on these intrinsic oscillations.(ABSTRACT TRUNCATED AT 400 WORDS)


2017 ◽  
Vol 2017 ◽  
pp. 1-10 ◽  
Author(s):  
D. Menniti ◽  
S. A. Pullano ◽  
M. G. Bianco ◽  
R. Citraro ◽  
E. Russo ◽  
...  

Relying on the mechanism of bat’s echolocation system, a bioinspired electronic device has been developed to investigate the cortical activity of mammals in response to auditory sensorial stimuli. By means of implanted electrodes, acoustical information about the external environment generated by a biomimetic system and converted in electrical signals was delivered to anatomically selected structures of the auditory pathway. Electrocorticographic recordings showed that cerebral activity response is highly dependent on the information carried out by ultrasounds and is frequency-locked with the signal repetition rate. Frequency analysis reveals that delta and beta rhythm content increases, suggesting that sensorial information is successfully transferred and integrated. In addition, principal component analysis highlights how all the stimuli generate patterns of neural activity which can be clearly classified. The results show that brain response is modulated by echo signal features suggesting that spatial information sent by biomimetic sonar is efficiently interpreted and encoded by the auditory system. Consequently, these results give new perspective in artificial environmental perception, which could be used for developing new techniques useful in treating pathological conditions or influencing our perception of the surroundings.


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