Adaptive Adjustment of Connectivity in the Inferior Colliculus Revealed by Focal Pharmacological Inactivation

2001 ◽  
Vol 85 (4) ◽  
pp. 1575-1584 ◽  
Author(s):  
Joshua I. Gold ◽  
Eric I. Knudsen
Keyword(s):  
Inferior Colliculus ◽  
Large Scale ◽  
Interaural Time Difference ◽  
Primary Source ◽  
Central Nucleus ◽  
Small Populations ◽  
Auditory Space ◽  
Adaptive Adjustment ◽  
Auditory Experience ◽  
Critical Site

In the midbrain sound localization pathway of the barn owl, a map of auditory space is synthesized in the external nucleus of the inferior colliculus (ICX) and transmitted to the optic tectum. Early auditory experience shapes these maps of auditory space in part by modifying the tuning of the constituent neurons for interaural time difference (ITD), a primary cue for sound-source azimuth. Here we show that these adaptive modifications in ITD tuning correspond to changes in the pattern of connectivity within the inferior colliculus. We raised owls with an acoustic filtering device in one ear that caused frequency-dependent changes in sound timing and level. As reported previously, device rearing shifted the representation of ITD in the ICX and tectum but not in the primary source of input to the ICX, the central nucleus of the inferior colliculus (ICC). We applied the local anesthetic lidocaine (QX-314) iontophoretically in the ICC to inactivate small populations of neurons that represented particular values of frequency and ITD. We measured the effect of this inactivation in the optic tecta of a normal owl and owls raised with the device. In the normal owl, inactivation at a critical site in the ICC eliminated responses in the tectum to the frequency-specific ITD value represented at the site of inactivation in the ICC. The location of this site was consistent with the known pattern of ICC-ICX-tectum connectivity. In the device-reared owls, adaptive changes in the representation of ITD in the tectum corresponded to dramatic and predictable changes in the locations of the critical sites of inactivation in the ICC. Given that the abnormal representation of ITD in the tectum depended on frequency and was likely conveyed directly from the ICX, these results suggest that experience causes large-scale, frequency-specific adjustments in the pattern of connectivity between the ICC and the ICX.

Responses of neurons in the auditory pathway of the barn owl to partially correlated binaural signals

1995 ◽  
Vol 74 (4) ◽  
pp. 1689-1700 ◽  
Author(s):  
Y. Albeck ◽  
M. Konishi
Keyword(s):  
Inferior Colliculus ◽  
Cross Correlation ◽  
Frequency Tuning ◽  
Neuronal Response ◽  
Interaural Time Difference ◽  
Central Nucleus ◽  
High Threshold ◽  
Correlation Model ◽  
Response Curves ◽  
The Cross

1. Extracellular single-unit recording in anesthetized barn owls was used to study neuronal response to dichotic stimuli of variable binaural correlation (BC). Recordings were made in the output fibers of nucleus laminaris (NL), the anterior division of the ventral lateral lemniscal nucleus (VLVa), the core of the central nucleus of the inferior colliculus (ICcC), the lateral shell of the central nucleus of the inferior colliculus (ICcLS), and the external nucleus of the inferior colliculus (ICx). 2. The response of all neurons sensitive to interaural time difference (ITD) varied with BC. The relationship between BC and impulse number fits a linear, a parabolic, or a ramp model. A linear or parabolic model fits most neurons in low-level nuclei. Higher order neurons in ICx did not respond to noise bursts with strong negative binaural correlation, creating a ramp-like response to BC. 3. A neuron's ability to detect ITD varied as a function of BC. Conversely, a neuron's response to BC changed with ITD. Neurons in NL, VLVa, and ICcC show almost periodic ITD response curves. In these neurons peaks and troughs of ITD response curves diminished as BC decreased, creating a flat ITD response when BC = 0. When BC was set to -1, the most favorable ITD became the least favorable one and vice versa. The ITD response curve of ICx neurons usually has a single dominant peak. The response of those neurons to a negatively correlated noise pair (BC = -1) showed two ITD peaks, flanking the position of the primary peak. 4. The parabolic BC response of NL neurons fits the prediction of the cross-correlation model, assuming half-wave rectification of the sound by the cochlea. Linear response is not predicted by the model. However, the parabolic and the linear neurons probably do not belong to two distinct groups as the difference between them is not statistically significant. Thus, the cross-correlation model provides a good description of the binaural response not only in NL but also in VLVa and ICcC. 5. Almost all ramp neurons occurred in either ICx or ICcLS where neurons are more broadly tuned to frequency than those in the lower nuclei. The synthesis of this response type requires, however, not only the convergence of different frequency channels but also inhibition between different ITD channels. We modeled the ramp response as a three-step process. First, different spectral channels converge to create broad frequency tuning. The response to variation in BC will be linear (or parabolic) because it is a sum of linear (parabolic) responses. Second, the activity in some adjacent ITD channels is subtracted by lateral inhibition. Finally, the result is rectified using a high threshold to avoid negative activity.

Adaptation in the Auditory Space Map of the Barn Owl

2006 ◽  
Vol 96 (2) ◽  
pp. 813-825 ◽  
Author(s):  
Yoram Gutfreund ◽  
Eric I. Knudsen
Keyword(s):  
Inferior Colliculus ◽  
Spatial Information ◽  
Short Term Memory ◽  
Threshold Level ◽  
Central Nucleus ◽  
Visually Guided ◽  
Auditory Space ◽  
Visual Spatial ◽  
Stimulus Offset ◽  
A Site

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.

Central and peripheral contributions to coding of acoustic space by neurons in inferior colliculus of cat

1986 ◽  
Vol 55 (3) ◽  
pp. 587-603 ◽  
Author(s):  
M. B. Calford ◽  
D. R. Moore ◽  
M. E. Hutchings
Keyword(s):  
Inferior Colliculus ◽  
Single Unit ◽  
Arrival Time ◽  
Interaural Time Difference ◽  
Free Field ◽  
Low Frequency ◽  
Intensity Function ◽  
Central Nucleus ◽  
Stimulus Position ◽  
Acoustic Space

Recordings of response to free-field stimuli at best frequency were made from single units in the central nucleus of the inferior colliculus of anesthetized cats. Stimulus position was varied in azimuth, and the responses of units were compared with variation in the intensity and arrival time of the sound at each ear, derived from cochlear microphonic (CM) recordings. CM recordings were made at each frequency and at every point in space for which single-unit data were collected. Interaural time difference (delay) increased monotonically, but not linearly, as the stimulus was moved away from the midline. However, a given delay did not represent a single azimuth across frequency. Low-frequency interaural intensity differences (IIDs) were monotonic across azimuth and peaked at, or near, the poles. Higher-frequency IIDs were nonmonotonic and peaked relatively close to the midline, decreasing toward the poles. Units that showed little variation in discharge across azimuth formed 28% of the sample and were classified as omnidirectional. For other units, the spike-count intensity function and the variation of the CM with azimuth were combined to form a derived monaural azimuth function. For 29% of those units showing azimuthal sensitivity, the derived monaural azimuth function matched the actual azimuth function. This suggested that these units received input from only one ear. The largest group of azimuthally sensitive units (47%) was formed from those units inferred to be IID sensitive. At higher frequencies these units displayed a peaked azimuth function paralleling the nonmonotonic relation of IID to azimuth. The proportion of inferred IID-sensitive units was close to that found in dichotic studies.

scholarly journals Emergence of Multiplicative Auditory Responses in the Midbrain of the Barn Owl

2007 ◽  
Vol 98 (3) ◽  
pp. 1181-1193 ◽  
Author(s):  
Brian J. Fischer ◽  
José Luis Peña ◽  
Masakazu Konishi
Keyword(s):  
Inferior Colliculus ◽  
Interaural Time Difference ◽  
Extracellular Recording ◽  
Auditory Pathway ◽  
Barn Owl ◽  
Central Nucleus ◽  
Interaural Level Difference ◽  
Tyto Alba ◽  
Neural Responses ◽  
Auditory Responses

Space-specific neurons in the barn owl's auditory space map gain spatial selectivity through tuning to combinations of the interaural time difference (ITD) and interaural level difference (ILD). The combination of ITD and ILD in the subthreshold responses of space-specific neurons in the external nucleus of the inferior colliculus (ICx) is well described by a multiplication of ITD- and ILD-dependent components. It is unknown, however, how ITD and ILD are combined at the site of ITD and ILD convergence in the lateral shell of the central nucleus of the inferior colliculus (ICcl) and therefore whether ICx is the first site in the auditory pathway where multiplicative tuning to ITD- and ILD-dependent signals occurs. We used extracellular recording of single neurons to determine how ITD and ILD are combined in ICcl of the anesthetized barn owl ( Tyto alba). A comparison of additive, multiplicative, and linear-threshold models of neural responses shows that ITD and ILD are combined nonlinearly in ICcl, but the interaction of ITD and ILD is not uniformly multiplicative over the sample. A subset (61%) of the neural responses is well described by the multiplicative model, indicating that ICcl is the first site where multiplicative tuning to ITD- and ILD-dependent signals occurs. ICx, however, is the first site where multiplicative tuning is observed consistently. A network model shows that a linear combination of ICcl responses to ITD–ILD pairs is sufficient to produce the multiplicative subthreshold responses to ITD and ILD seen in ICx.

scholarly journals Preservation of Spectrotemporal Tuning Between the Nucleus Laminaris and the Inferior Colliculus of the Barn Owl

2007 ◽  
Vol 97 (5) ◽  
pp. 3544-3553 ◽  
Author(s):  
G. Björn Christianson ◽  
José Luis Peña
Keyword(s):  
Inferior Colliculus ◽  
Phase Locking ◽  
Interaural Time Difference ◽  
Barn Owl ◽  
Central Nucleus ◽  
Sound Recognition ◽  
Spectral Structure ◽  
Two Stages ◽  
The Brain ◽  
Ongoing Phase

Performing sound recognition is a task that requires an encoding of the time-varying spectral structure of the auditory stimulus. Similarly, computation of the interaural time difference (ITD) requires knowledge of the precise timing of the stimulus. Consistent with this, low-level nuclei of birds and mammals implicated in ITD processing encode the ongoing phase of a stimulus. However, the brain areas that follow the binaural convergence for the computation of ITD show a reduced capacity for phase locking. In addition, we have shown that in the barn owl there is a pooling of ITD-responsive neurons to improve the reliability of ITD coding. Here we demonstrate that despite two stages of convergence and an effective loss of phase information, the auditory system of the anesthetized barn owl displays a graceful transition to an envelope coding that preserves the spectrotemporal information throughout the ITD pathway to the neurons of the core of the central nucleus of the inferior colliculus.

Response of auditory units in the barn owl's inferior colliculus to continuously varying interaural phase differences

1992 ◽  
Vol 67 (6) ◽  
pp. 1428-1436 ◽  
Author(s):  
A. Moiseff ◽  
T. Haresign
Keyword(s):  
Inferior Colliculus ◽  
Interaural Time Difference ◽  
Stimulus Onset ◽  
Central Nucleus ◽  
Intensity Difference ◽  
Phase Sensitivity ◽  
Tyto Alba ◽  
Interaural Phase ◽  
Stimulus Generation ◽  
Phase Differences

1. We studied the response of single units in the central nucleus of the inferior colliculus (ICc) of the barn owl (Tyto alba) to continuously varying interaural phase differences (IPDs) and static IPDs. Interaural phase was varied in two ways: continuously, by delivering tones to each ear that varied by a few hertz (binaural beat, Fig. 1), and discretely, by delaying in fixed steps the phase of sound delivered to one ear relative to the other (static phase). Static presentations were repeated at several IPDs to characterize interaural phase sensitivity. 2. Units sensitive to IPDs responded to the binaural beat stimulus over a broad range of delta f(Fig. 4). We selected a 3-Hz delta f for most of our comparative measurements on the basis of constraints imposed by our stimulus generation system and because it allowed us to reduce the influence of responses to stimulus onset and offset (Fig. 3A). 3. Characteristic interaural time or phase sensitivity obtained by the use of the binaural beat stimulus were comparable with those obtained by the use of the static technique (Fig. 5; r2 = 0.93, Fig. 6). 4. The binaural beat stimulus facilitated the measurement of characteristic delay (CD) and characteristic phase (CP) of auditory units. We demonstrated that units in the owl's inferior colliculus (IC) include those that are maximally excited by specific IPDs (CP = 0 or 1.0) as well as those that are maximally suppressed by specific IPDs (CP = 0.5; Figs. 7 and 8). 5. The selectivity of units sensitive to IPD or interaural time difference (ITD) were weakly influenced by interaural intensity difference (IID).(ABSTRACT TRUNCATED AT 250 WORDS)

scholarly journals Alignment of sound localization cues in the nucleus of the brachium of the inferior colliculus

2014 ◽  
Vol 111 (12) ◽  
pp. 2624-2633 ◽  
Author(s):  
Sean J. Slee ◽  
Eric D. Young
Keyword(s):  
Inferior Colliculus ◽  
Sound Localization ◽  
Additive Model ◽  
Central Nucleus ◽  
Intensity Difference ◽  
Auditory Space ◽  
Directional Filtering ◽  
Spectral Cues ◽  
Spatial Alignment ◽  
Auditory Space Map

Accurate sound localization is based on three acoustic cues (interaural time and intensity difference and spectral cues from directional filtering by the pinna). In natural listening conditions, every spatial position of a sound source provides a unique combination of these three cues in “natural alignment.” Although neurons in the central nucleus (ICC) of the inferior colliculus (IC) are sensitive to multiple cues, they do not favor their natural spatial alignment. We tested for sensitivity to cue alignment in the nucleus of the brachium of the IC (BIN) in unanesthetized marmoset monkeys. The BIN receives its predominant auditory input from ICC and projects to the topographic auditory space map in the superior colliculus. Sound localization cues measured in each monkey were used to synthesize broadband stimuli with aligned and misaligned cues; spike responses to these stimuli were recorded in the BIN. We computed mutual information (MI) between the set of spike rates and the stimuli containing either aligned or misaligned cues. The results can be summarized as follows: 1) BIN neurons encode more information about auditory space when cues are aligned compared with misaligned. 2) Significantly more units prefer aligned cues in the BIN than in ICC. 3) An additive model based on summing the responses to stimuli with the localization cues varying individually accurately predicts the alignment preference with all cues varying. Overall, the results suggest that the BIN is the first site in the ascending mammalian auditory system that is tuned to natural combinations of sound localization cues.

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