scholarly journals Differing Roles of Inhibition in Hierarchical Processing of Species-Specific Calls in Auditory Brainstem Nuclei

2005 ◽  
Vol 94 (6) ◽  
pp. 4019-4037 ◽  
Author(s):  
Ruili Xie ◽  
John Meitzen ◽  
George D. Pollak
Keyword(s):  
Auditory Brainstem ◽  
Lateral Lemniscus ◽  
Response Properties ◽  
Hierarchical Processing ◽  
Tuning Curves ◽  
Neuronal Populations ◽  
Dorsal Nucleus ◽  
Brainstem Nuclei ◽  
Communication Calls ◽  
Species Specific

Here we report on response properties and the roles of inhibition in three brain stem nuclei of Mexican-free tailed bats: the inferior colliculus (IC), the dorsal nucleus of the lateral lemniscus (DNLL) and the intermediate nucleus of the lateral lemniscus (INLL). In each nucleus, we documented the response properties evoked by both tonal and species-specific signals and evaluated the same features when inhibition was blocked. There are three main findings. First, DNLL cells have little or no surround inhibition and are unselective for communication calls, in that they responded to ∼97% of the calls that were presented. Second, most INLL neurons are characterized by wide tuning curves and are unselective for species-specific calls. The third finding is that the IC population is strikingly different from the neuronal populations in the INLL and DNLL. Where DNLL and INLL neurons are unselective and respond to most or all of the calls in the suite we presented, most IC cells are selective for calls and, on average, responded to ∼50% of the calls we presented. Additionally, the selectivity for calls in the majority of IC cells, as well as their tuning and other response properties, are strongly shaped by inhibitory innervation. Thus we show that inhibition plays only limited roles in the DNLL and INLL but dominates in the IC, where the various patterns of inhibition sculpt a wide variety of emergent response properties from the backdrop of more expansive and far less specific excitatory innervation.

Differential Response Properties to Amplitude Modulated Signals in the Dorsal Nucleus of the Lateral Lemniscus of the Mustache Bat and the Roles of GABAergic Inhibition

1997 ◽  
Vol 77 (1) ◽  
pp. 324-340 ◽  
Author(s):  
Lichuan Yang ◽  
George D. Pollak
Keyword(s):  
Phase Locking ◽  
Modulation Frequency ◽  
Tone Burst ◽  
Differential Response ◽  
Gabaergic Inhibition ◽  
Lateral Lemniscus ◽  
Response Properties ◽  
Dorsal Nucleus ◽  
Modulated Signals ◽  
Onset Response

Yang, Lichuan and George D. Pollak. Differential response properties to amplitude modulated signals in the dorsal nucleus of the lateral lemniscus of the mustache bat and the roles of GABAergic inhibition. J. Neurophysiol. 77: 324–340, 1997. We studied the phase-locking of 89 neurons in the dorsal nucleus of the lateral lemniscus (DNLL) of the mustache bat to sinusoidally amplitude modulated (SAM) signals and the influence that GABAergic inhibition had on their response properties. Response properties were determined with tone bursts at each neuron's best frequency and then with a series of SAM signals that had modulation frequencies ranging from 50–100 to 800 Hz in 100-Hz steps. DNLL neurons were divided into two principal types: sustained neurons (55%), which responded throughout the duration of the tone burst, and onset neurons (45%), which responded only at the beginning of the tone burst. Sustained and onset neurons responded differently to SAM signals. Sustained neurons responded with phase-locked discharges to modulation frequencies ≤400–800 Hz. In contrast, 70% of the onset neurons phase-locked only to low modulation frequencies of 100–300 Hz, whereas 30% of the onset neurons did not phase-lock to any modulation frequency. Signal intensity differentially affected the phase-locking of sustained and onset neurons. Sustained neurons exhibited tight phase-locking only at low intensities, 10–30 dB above threshold. Onset neurons, in contrast, maintained strong phase-locking even at relatively high intensities. Blocking GABAergic inhibition with bicuculline had different effects on the phase-locking of sustained and onset neurons. In sustained neurons, there was an overall decline in phase-locking at all modulation frequencies. In contrast, 70% of the onset neurons phase-locked to much higher modulation frequencies than they did when inhibition was intact. The other 30% of onset neurons phase-locked to SAM signals, although they fired only with an onset response to the same signals before inhibition was blocked. In both cases, blocking GABAergic inhibition transformed their responses to SAM signals into patterns that were more like those of sustained neurons. We also propose mechanisms that could explain the differential effects of GABAergic inhibition on onset neurons that locked to low modulation frequencies and on onset neurons that did not lock to any SAM signals before inhibition was blocked. The key features of the proposed mechanisms are the absolute latencies and temporal synchrony of the excitatory and inhibitory inputs.

Axon Trajectories in the Auditory Brainstem

2019 ◽  
pp. 472-502
Author(s):  
Nell Beatty Cant
Keyword(s):  
White Matter ◽  
Auditory Brainstem ◽  
Current Level ◽  
Fiber Bundles ◽  
Lateral Lemniscus ◽  
Physiological Studies ◽  
Level Of Understanding ◽  
Species Specific ◽  
Trapezoid Body

This chapter summarizes what is known about the organization of the axons that make up the white matter of the auditory brainstem. The sources of the axons in each of the major fiber bundles (the dorsal and intermediate acoustic striae, the ventral acoustic stria or trapezoid body, and the lateral lemniscus) are reviewed, and, where information is available, the organization of specific groups of axons within the fiber bundles is described. The chapter collects the extensive but scattered information about axon trajectories into one place, both to provide a summary of what is known and also to indicate important gaps in our knowledge. The emphasis is almost entirely on the routes followed by groups of axons over the relatively long distances between structures and on the organization of specific types of axons within the fiber bundles; information about the termination patterns of the axons can be obtained from the references cited and throughout the chapter. Because knowledge about axon trajectories has considerable practical value (as, for example, in designing and interpreting both anatomical and physiological studies), the most useful information is species specific. Fortunately, at least at our current level of understanding, the components and relative positions of the major fiber bundles are remarkably similar across species (undoubtedly reflecting a common mammalian developmental plan).

Binaural Response Properties of Low-Frequency Neurons in the Gerbil Dorsal Nucleus of the Lateral Lemniscus

2006 ◽  
Vol 96 (3) ◽  
pp. 1425-1440 ◽  
Author(s):  
Ida Siveke ◽  
Michael Pecka ◽  
Armin H. Seidl ◽  
Sylvie Baudoux ◽  
Benedikt Grothe
Keyword(s):  
Low Frequency ◽  
Superior Olivary Complex ◽  
Suitable Model ◽  
Medial Superior Olive ◽  
Lateral Lemniscus ◽  
Auditory Midbrain ◽  
Response Properties ◽  
Superior Olive ◽  
Dorsal Nucleus ◽  
Anatomical Evidence

Differences in intensity and arrival time of sounds at the two ears, interaural intensity and time differences (IID, ITD), are the chief cues for sound localization. Both cues are initially processed in the superior olivary complex (SOC), which projects to the dorsal nucleus of the lateral lemniscus (DNLL) and the auditory midbrain. Here we present basic response properties of low-frequency (<2 kHz) DNLL neurons and their binaural sensitivity to ITDs and IIDs in the anesthetized gerbil. We found many neurons showing binaural properties similar to those reported for SOC neurons. IID-properties were similar to that of the contralateral lateral superior olive (LSO). A majority of cells had an ITD sensitivity resembling that of either the ipsilateral medial superior olive (MSO) or the contralateral LSO. A smaller number of cells displayed intermediate types of ITD sensitivity. In neurons with MSO-like response ITDs that evoked maximal discharges were mostly outside of the range of ITDs the gerbil naturally experiences. The maxima of the first derivative of their ITD-functions (steepest slope), however, were well within the physiological range of ITDs. This finding is consistent with the concept of a population rather than a place code for ITDs. Moreover, we describe several other binaural properties as well as physiological and anatomical evidence for a small but significant input from the contralateral MSO. The large number of ITD-sensitive low-frequency neurons implicates a substantial role for the DNLL in ITD processing and promotes this nucleus as a suitable model for further studies on ITD-coding.

Response properties of single units in the dorsal nucleus of the lateral lemniscus and paralemniscal zone of an echolocating bat

1993 ◽  
Vol 69 (3) ◽  
pp. 842-859 ◽  
Author(s):  
E. Covey
Keyword(s):  
Sound Level ◽  
Single Units ◽  
Superior Olivary Complex ◽  
Inhibitory Input ◽  
Gamma Aminobutyric Acid ◽  
Lateral Lemniscus ◽  
Response Properties ◽  
Binaural Interaction ◽  
Dorsal Nucleus ◽  
Interaural Level Differences

1. Connectional evidence suggests that the dorsal nucleus of the lateral lemniscus (DNLL) and the paralemniscal zone (PL) function as centers for binaural analysis interposed between the superior olivary complex and the midbrain. In addition, the DNLL is known to be a major source of inhibitory input to the midbrain. The aim of this study was to characterize the response properties of neurons in DNLL and PL of the echolocating bat Eptesicus fuscus, a species that utilizes high-frequency hearing and that might be expected to have a large proportion of neurons responsive to interaural differences in sound level. 2. Auditory stimuli were presented monaurally or binaurally to awake animals, and responses of single units were recorded extra-cellularly with the use of glass micropipettes. 3. Below the ventrolateral border of the inferior colliculus is a region that contains large gamma-aminobutyric acid-positive neurons. On the basis of its immunohistochemical reactivity, this entire region could be considered as DNLL. However, within the area, there was an uneven distribution of binaural responses. Caudally, binaural neurons made up 84% (41/49) of those tested, but rostrally only 29% (6/21). For this reason the rostral area is considered as a separate functional subdivision and referred to as the dorsal paralemniscal zone (DPL). PL is located ventral to DPL and medial to the intermediate and ventral nuclei of the lateral lemniscus; in PL 88% (14/16) of neurons were binaural. 4. Most neurons responded only to a contralateral stimulus when sounds were presented monaurally. Out of 49 neurons in DNLL, 42 responded only to a contralateral sound, 1 responded only to an ipsilateral sound, and 6 responded to sound at either ear. In the DPL, all of the 21 neurons tested responded to a contralateral sound and none to an ipsilateral sound. Out of 16 neurons in the PL, 11 responded only to a contralateral sound, 1 responded only to an ipsilateral sound, and 4 responded to sound at either ear. 5. When sounds were presented at both ears simultaneously, several different patterns of binaural interaction occurred. The most common pattern was suppression of the response to sound at one ear by sound at the other ear. In DNLL, 57% (28/49) of neurons showed this type of binaural interaction. Another 10% (5/49) showed facilitation at some interaural level differences and suppression at others, and another 10% (5/49) showed facilitation at some interaural level differences but no suppression.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Response Properties of Single Units in the Dorsal Nucleus of the Lateral Lemniscus of Decerebrate Cats

2007 ◽  
Vol 98 (3) ◽  
pp. 1475-1488 ◽  
Author(s):  
Kevin A. Davis ◽  
Oleg Lomakin ◽  
Michael J. Pesavento
Keyword(s):  
Broadband Noise ◽  
Type I ◽  
Lateral Lemniscus ◽  
Decerebrate Cat ◽  
Response Properties ◽  
Dorsal Nucleus ◽  
Contralateral Response ◽  
High Level ◽  
Interaural Level Differences ◽  
Type V

The dorsal nucleus of the lateral lemniscus (DNLL) receives afferent inputs from many brain stem nuclei and, in turn, is a major source of inhibitory inputs to the inferior colliculus (IC). The goal of this study was to characterize the monaural and binaural response properties of neurons in the DNLL of unanesthetized decerebrate cat. Monaural responses were classified according to the patterns of excitation and inhibition observed in contralateral and ipsilateral frequency response maps. Binaural classification was based on unit sensitivity to interaural level differences. The results show that units in the DNLL can be grouped into three distinct types. Type v units produce contralateral response maps that show a wide V-shaped excitatory area and no inhibition. These units receive ipsilateral excitation and exhibit binaural facilitation. The contralateral maps of type i units show a more restricted I-shaped region of excitation that is flanked by inhibition. Type o maps display an O-shaped island of excitation at low stimulus levels that is bounded by inhibition at higher levels. Both type i and type o units receive ipsilateral inhibition and exhibit binaural inhibition. Units that produce type v maps have a low best frequency (BF), whereas type i and type o units have high BFs. Type v and type i units give monotonic rate-level responses for both BF tones and broadband noise. Type o units are inhibited by tones at high levels, but are excited by high-level noise. These results show that the DNLL can exert strong, differential effects in the IC.

The Nuclei of the Lateral Lemniscus

2019 ◽  
pp. 444-472
Author(s):  
Felix Felmy
Keyword(s):  
Inferior Colliculus ◽  
Auditory Processing ◽  
Fiber Bundle ◽  
Auditory Brainstem ◽  
Superior Olivary Complex ◽  
Auditory Information ◽  
Lateral Lemniscus ◽  
Sound Sources ◽  
Dorsal Nucleus ◽  
The Individual

Parallel processing streams guide ascending auditory information through the processing hierarchy of the auditory brainstem. Many of these processing streams converge in the lateral lemnisucus, the fiber bundle that connects the cochlear nuclei and superior olivary complex with the inferior colliculus. The neuronal populations within the lateral lemniscus can be segregated according to their gross structure-function relationships into three distinct nuclei. These nuclei are termed ventral, intermedial, and dorsal nucleus, according to their position within the lemniscal fiber bundle. The complexity of their input pattern increases in an ascending fashion. The three nuclei employ different neurotransmitters and exhibit distinct synaptic and biophysical features. Yet they all share a large heterogeneity. Functionally, the ventral nucleus of the lateral lemniscus has been hypothesized to reduce spectral splatter by generating a rapid, temporally precise feedforward onset inhibition in the inferior colliculus. In the intermedial nucleus of the lateral lemniscus a cross-frequency integration has been observed. The hallmark of the dorsal nucleus of the lateral lemniscus is the generation of a long-lasting inhibition in its contralateral counterpart and the inferior colliculus. This inhibition is proposed to generate a suppression of sound sources during reverberations and could act as a temporal filter capable of removing spurious interaural time differences. While great advances have been made in understanding the role that these nuclei play in auditory processing, the functional diversity of the individual neuronal responsiveness within each nucleus remains largely unsolved.

Spectral Determination of Responses to Species-Specific Calls in the Dorsal Nucleus of the Lateral Lemniscus

2002 ◽  
Vol 88 (4) ◽  
pp. 1955-1967 ◽  
Author(s):  
Eric E. Bauer ◽  
Achim Klug ◽  
George D. Pollak
Keyword(s):  
Tone Burst ◽  
Similar Response ◽  
Spectral Determination ◽  
Lateral Lemniscus ◽  
Complex Sounds ◽  
Dorsal Nucleus ◽  
Temporal Features ◽  
Response Profiles ◽  
Discharge Patterns ◽  
Species Specific

This study evaluated how neurons in the dorsal nucleus of the lateral lemniscus (DNLL) in Mexican free-tailed bats respond to both tone bursts and species-specific calls. Up to 20 calls were presented to each neuron, of which 18 were social communication and 2 were echolocation calls. We also measured excitatory response regions (ERRs): the range of tone burst frequencies that evoked discharges at a fixed intensity. Neurons were unselective for one or another call in that each neuron responded to any call so long as the call had energy that encroached on its ERR. Additionally, responses were evoked by the same set of calls, and with similar spike counts, when they were presented normally or reversed. By convolving activity in the ERRs with the spectrogram of each call, we showed that responses to tones accurately predicted discharge patterns evoked by species-specific calls. DNLL cells are remarkably homogeneous in that neurons having similar BFs responded to each of the species-specific calls with similar response profiles. The homogeneity was further illustrated by the ability to accurately predict the response profiles of a particular DNLL cell to species-specific calls from the ERR of another similarly tuned DNLL cell. Thus DNLL neurons tuned to the same or similar frequencies responded to species-specific calls with latencies and temporal discharge patterns that were so similar as to be virtually interchangeable. What this suggests is that DNLL responses evoked by complex sounds can be largely explained by a simple summation of the excitation in each neuron's ERR. Finally, superimposing the spectrograms of each call on the responses evoked by that call revealed that the DNLL population response re-creates both the spectral and the temporal features of each signal.

Sign in / Sign up

Export Citation Format

Share Document