Responses of Neurons in the Rat's Ventral Nucleus of the Lateral Lemniscus to Monaural and Binaural Tone Bursts

Abstract

Zhang, Huiming and Jack B. Kelly. Responses of neurons in the rat's ventral nucleus of the lateral lemniscus to monaural and binaural tone bursts. J Neurophysiol 95: 2501-2512, 2006. First published January 4, 2006 doi:10.1152/jn.01215.2005. Responses to monaural and binaural tone bursts were recorded from neurons in the rat's ventral nucleus of the lateral lemniscus (VNLL). Most of the neurons (55%) had V-or U-shaped frequency-tuning curves with a single clearly defined characteristic frequency (CF). However, many neurons had more complex, multipeaked tuning curves (37%), or other patterns (8%). Temporal firing patterns included both onset and sustained responses to contralateral tone bursts. Onset and sustained responses were distributed along the dorsoventral length of VNLL with no indication of segregation into different regions. Onset neurons had shorter average first-spike latencies than neurons with sustained responses (means, 8.3 vs. 14.8 ms). They also had less jitter, as reflected in the SD of first-spike latencies, than neurons with sustained responses (means, 0.59 and 4.2 ms, respectively). The extent of jitter decreased with an increase in stimulus intensity for neurons with sustained responses, but remained unchanged for onset neurons tested over the same range. Many neurons had binaural responses, primarily of the excitatory/inhibitory (EI) type, widely distributed along the dorsoventral extent of VNLL. Local application of the AMPA receptor antagonist NBQX reduced excitatory responses, indicating that responses were dependent on synaptic activity and not recorded from passing fibers. The results show that many neurons in VNLL have a precision of timing that is well suited for processing auditory temporal information. In the rat, these neurons are intermingled among cells with less precise temporal response features and include cells with binaural as well as monaural responses. I N T R O D U C T I O NThe ventral nucleus of the lateral lemniscus (VNLL), a prominent structure in the auditory brain stem, consists of a discrete collection of neurons located along the pathway from cochlear nucleus to inferior colliculus. The VNLL receives major afferent projections from the contralateral ventral cochlear nucleus (VCN), the ipsilateral medial nucleus of the trapezoid body (MNTB), and other ipsilateral periolivary nuclei, but does not receive projections from the medial or lateral superior olives, two nuclei that have been shown to be important for binaural processing in the auditory system

Temporal properties of responses to sound in the ventral nucleus of the lateral lemniscus

“…The proportion of VNLL neurons considered binaural was relatively small in Aitkin et al (1970) and Covey and Casseday (1991) but was larger (50%) in our sample, as in Guinan et al (1972aGuinan et al ( , 1972b and in other recent studies (Batra andFitzpatrick 1999, 2002a;Zhang and Kelly 2006a). Binaural interaction was shown to be weak, however, particularly compared with the LSO (Fig.…”

“…Early studies of the VNLL were conflicting regarding the extent of its binaural properties (Aitkin et al 1970;Guinan et al 1972aGuinan et al , 1972b. Recent work confirms that sensitivity to ILDs is present in this nucleus in rabbits and rats (Batra and Fitzpatrick 1999;Zhang and Kelly 2006a) but not in bats (Covey and Casseday 1991). We obtained ILD functions by presenting contralateral pure tones at CF at a fixed suprathreshold level 20 -40 dB re threshold.…”

“…There was a cluster of cells with CF Ͻ 2 kHz, but very few cells below 1 kHz. A high-CF bias (compared to the behavioral audiogram) is also present in the rat (Zhang and Kelly 2006a). This is perhaps less obvious in the rabbit (Batra and Fitzpatrick 1999), although even there very few neurons with CF Ͻ 700 Hz were present.…”

“…In this region, neurons have a first-spike latency that is rather invariant across trials and stimulus levels and that is assumed to play a role in the encoding of sound onsets Casseday 1986, 1991). Recent work in rabbit (Batra and Fitzpatrick 2002a) and rat (Nayagam et al 2005(Nayagam et al , 2006Zhang and Kelly 2006a) shows that responses to pure tones in these animals resemble those found in the bat. Of special interest are responses to sinusoidally amplitude-modulated (SAM) tones (Batra 2006;Zhang and Kelly 2006b), which indicate the existence of neurons that are narrowly tuned to different modulation frequencies.…”

First-spike latency information in single neurons increases when referenced to population onset

“…They respond strongly to modulated stimuli and thus mark temporal features of sounds, such as the syllables of speech. Octopus cells project to an area of the contralateral ventral nucleus of the lateral lemniscus (VnLL) that also contains onset neurons (32)(33)(34); the VnLL, in turn, projects to the IC, often making inhibitory terminals (35). Both sets of onset cells have properties consistent with a population marker for stimulus onsets.…”