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

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.

2007 ◽  
Vol 97 (5) ◽  
pp. 3544-3553 ◽  
Author(s):  
G. Björn Christianson ◽  
José Luis Peña

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.


1992 ◽  
Vol 67 (6) ◽  
pp. 1428-1436 ◽  
Author(s):  
A. Moiseff ◽  
T. Haresign

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)


1995 ◽  
Vol 74 (4) ◽  
pp. 1689-1700 ◽  
Author(s):  
Y. Albeck ◽  
M. Konishi

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.


1975 ◽  
Vol 38 (5) ◽  
pp. 1208-1216 ◽  
Author(s):  
L. M. Aitkin ◽  
D. R. Moore

Tuning curves were measured for 65 units in the inferior colliculus of seven anesthetized kittens aged from 6 to 28 days. At 2 days of age the inferior colliculus was divisible into central, pericentral, and external nuclei. Evidence was found for broader tuning curves to occur in the pericentral nucleus compared with the central nucleus, as has been observed in the adult. The middle ear was filled with serous fluid to 6 days, while the external auditory meatus remained collapsed until 10 days. Central nucleus tuning curves in kittens were relatively flat with high thresholds. Best-frequency thresholds diminished from a mean of near 100 dB SPL at 6-11 days to near 50 dB in the adult. The marked drop in thresholds between days 22 and 21 led to the adoption of the sharp form of tuning curve common for adults. Tonotopic organization of the central nucleus was clear at day 11. Speculations were advanced about the dependence of central auditory maturations on cochlear development, axon myelination in the auditory pathway, and changes in synaptic density as a function of age.


2009 ◽  
Vol 102 (1) ◽  
pp. 167-180 ◽  
Author(s):  
Donald Gans ◽  
Kianoush Sheykholeslami ◽  
Diana Coomes Peterson ◽  
Jeffrey Wenstrup

This report examines temporal features of facilitation and suppression that underlie spectrally integrative responses to complex vocal signals. Auditory responses were recorded from 160 neurons in the inferior colliculus (IC) of awake mustached bats. Sixty-two neurons showed combination-sensitive facilitation: responses to best frequency (BF) signals were facilitated by well-timed signals at least an octave lower in frequency, in the range 16–31 kHz. Temporal features and strength of facilitation were generally unaffected by changes in duration of facilitating signals from 4 to 31 ms. Changes in stimulus rise time from 0.5 to 5.0 ms had little effect on facilitatory strength. These results suggest that low frequency facilitating inputs to high BF neurons have phasic-on temporal patterns and are responsive to stimulus rise times over the tested range. We also recorded from 98 neurons showing low-frequency (11–32 kHz) suppression of higher BF responses. Effects of changing duration were related to the frequency of suppressive signals. Signals <23 kHz usually evoked suppression sustained throughout signal duration. This and other features of such suppression are consistent with a cochlear origin that results in masking of responses to higher, near-BF signal frequencies. Signals in the 23- to 30-kHz range—frequencies in the first sonar harmonic—generally evoked phasic suppression of BF responses. This may result from neural inhibitory interactions within and below IC. In many neurons, we observed two or more forms of the spectral interactions described here. Thus IC neurons display temporally and spectrally complex responses to sound that result from multiple spectral interactions at different levels of the ascending auditory pathway.


1986 ◽  
Vol 55 (3) ◽  
pp. 587-603 ◽  
Author(s):  
M. B. Calford ◽  
D. R. Moore ◽  
M. E. Hutchings

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.


2008 ◽  
Vol 100 (2) ◽  
pp. 708-715 ◽  
Author(s):  
Brian J. Fischer ◽  
Masakazu Konishi

The interaural time difference (ITD) is the primary auditory cue used by the barn owl for localization in the horizontal direction. ITD is initially computed by circuits consisting of axonal delay lines from one of the cochlear nuclei and coincidence detector neurons in the nucleus laminaris (NL). NL projects directly to the anterior part of the dorsal lateral lemniscal nucleus (LLDa), and this area projects to the core of the central nucleus of the inferior colliculus (ICcc) in the midbrain. To show the selectivity of an NL neuron for ITD requires averaging of responses over several stimulus presentations for each ITD. In contrast, ICcc neurons detect their preferred ITD in a single burst of stimulus. We recorded extracellularly the responses of LLDa neurons to ITD in anesthetized barn owls and show that this ability is already present in LLDa, raising the possibility that ICcc inherits its noise reduction property from LLDa.


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