Monaural spectral processing differs between the lateral superior olive and the inferior colliculus: Physiological evidence for an acoustic chiasm

Abstract

Evidence suggests that the lateral superior olive (LSO) initiates an excitatory pathway specialized to process interaural level differences (ILDs), the primary cues used by mammals to localize highfrequency sounds in the horizontal plane. Type I units in the central nucleus of the inferior colliculus (ICC) of decerebrate cats exhibit monaural and binaural response properties qualitatively similar to those of LSO units, and are thus supposed to be the midbrain component of the ILD pathway. Studies have shown, however, that the responses of ICC cells do not often reflect simply the output of any single source of excitatory inputs. The goal of this study was to compare directly the monaural, spectral response properties of LSO and type I units measured in unanesthetized decerebrate cats. Compared to LSO units, type I units have narrower V-shaped excitatory tuning curves, higher spontaneous rates, lower maximum stimulus-evoked firing rates and more nonmonotonic rate-level curves for tones and noise. In addition, low frequency type I units have lower thresholds to tones than corresponding LSO units. Taken together, these results suggest that the excitatory ILD pathway from LSO to ICC is mostly a high-frequency channel, and that additional inputs transform LSO influences in the ICC.

Frequency response areas in the inferior colliculus: nonlinearity and binaural interaction

“…The classification scheme applied in this study is based on spectral tuning for tones (Ramachandran et al, 1999; Greene et al, 2010), analysis of masking patterns (Ramachandran et al, 2000), and binaural processing (Davis et al, 1999; Ramachandran and May, 2002). The validity of this scheme is supported by the fact that class definitions incorporate multiple aspects of a neuron's response properties.…”

Evidence of a Functionally Segregated Pathway from Lateral Superior Olive to Inferior Colliculus

“…Details of the surgical preparation are described elsewhere (Greene et al 2010). Briefly, adult male cats (3-4 kg) with infection-free ears were anesthetized with ketamine (initial/supplemental dose 40/20 mg/kg im) and xylazine (0.5/0.25 mg/kg im), and given atropine (0.05 mg/kg im) to minimize respiratory secretions and dexamethasone (2 mg/kg im) to reduce cerebral edema.…”

“…Placement of the injection electrode was completed using a two-step process. First, to locate the LSO, platinum-iridium metal electrodes were advanced through the brain stem using a standardized dorsoventral approach (Greene et al 2010) while 50-ms search stimuli were presented to the excitatory ear (ipsilateral for LSO, contralateral for ICC). When the LSO is approached from this direction, unit BFs tend to increase with depth in its medial and lateral limbs (the BFs are higher in the medial limb), but decrease in its central limb (Tsuchitani and Boudreau 1966).…”

“…The location of the LSO was verified based upon histological confirmation in one early experiment, but usually upon electrode position (3-4 mm lateral from the midline; 5-6 mm below the floor of the fourth ventricle), progression of unit BFs and similarity of single-unit monaural (tuning curve shape and width, maximum and spontaneous discharge rates) and binaural (i.e. EI) response properties to published data (Finlayson and Caspary 1991; Greene et al 2010; Guinan et al 1972a; Guinan et al 1972b; Tollin and Yin 2005; Tsuchitani 1977). Note that a chopping response in the post-stimulus time histogram is not a defining characteristic of LSO units in decerebrate cat (Brownell et al 1979; Greene and Davis 2012), thus was not used to identify LSO units here.…”

“…The existence of ICC unit types with distinct receptive field properties has led to the proposal that ICC response types are derived from different sources of ascending input that remain functionally segregated within the midbrain (Ramachandran et al 1999). In particular, it has been speculated that type I units receive their primary excitatory input from principal cells in the lateral superior olive (LSO) (Caird and Klinke 1983; Greene et al 2010), type V units are shaped by inputs from the medial superior olive (MSO) (Goldberg and Brown 1969; Guinan et al 1972a; b; Yin and Chan 1990), and that type O units reflect inputs from the dorsal cochlear nucleus (DCN) (Spirou and Young 1991; Young and Brownell 1976). Consistent with this connectionist model, inputs to the ICC form distinct nucleotopic synaptic domains (Oliver and Huerta 1992), unit classification of ICC neurons is not strongly modified by local pharmacological manipulations (Davis 1999; 2002), and each ICC unit type shares the binaural response properties of its putative input (Davis 2002; Ramachandran and May 2002).…”