Inhibitory projections from the ventral nucleus of the lateral lemniscus and superior paraolivary nucleus create directional selectivity of frequency modulations in the inferior colliculus: a comparison of bats with other mammals

Abstract

This review considers four auditory brainstem nuclear groups and shows how studies of both bats and other mammals have provided insights into their response properties and the impact of their convergence in the inferior colliculus (IC). The four groups are octopus cells in the cochlear nucleus, their connections with the ventral nucleus of the lateral lemniscus (VNLL) and the superior paraolivary nucleus (SPON), and the connections of the VNLL and SPON with the IC. The theme is that the response properties of neurons in the SPON and VNLL map closely onto the synaptic response features of a unique subpopulation of cells in the IC of bats whose inputs are dominated by inhibition. We propose that the convergence of VNLL and SPON inputs generates the tuning of these IC cells, their unique temporal responses to tones, and their directional selectivities for frequency modulated (FM) sweeps. Other IC neurons form directional properties in other ways, showing that selective response properties are formed in multiple ways. In the final section we discuss why multiple formations of common response properties could amplify differences in population activity patterns evoked by signals that have similar spectrotemporal features.

Fig. 1

Circuitry and features of VNLLc cells. A: circuit showing projections to VNLLc from octopus cells in the cochlear nucleus and from MNTB cells. Redrawn from Vater, M., Covey, E., and Casseday, J.H. (1997). The columnar region of the ventral nucleus of the lateral lemniscus in the big brown bat (Eptesicus fuscus): synaptic arrangements and structural correlates of feed-forward inhibitory function. Cell Tissue Res 289:223–233. By permission of Springer-Verlag. B: End-bulbs of Held from octopus cells terminate on spherical cells in VNLLc. Adapted from Vater, M. and Feng, A.S. (1990) Functional organization of ascending and descending connections of the cochlear nucleus of horseshoe bats. J Comp Neurol 292:373–395. By permission of John Wiley & Sons. C: Responses of VNLLc cell to tone bursts. Top is raster display of responses evoked by tones while lower record shows same responses displayed as a PST histogram. D: Immunostained sections of the VNLLc from mustache bats showing that all neurons stain intensely for glycine but not GABA. Adapted from Winer, J.A., Larue, D.T. and Pollak, G.D. (1995) GABA and glycine in the central auditory system of the mustache bat: structural substrates for inhibitory neuronal organization. J Comp Neurol 355:317–353. By permission of John Wiley & Sons.

Fig. 2

Connections and tone evoked responses in SPON cells. A: Connectional basis for tone evoked off responses. SPON cells receive tonic excitation from stellate cells and a tonic inhibition from MNTB that suppresses discharges for the duration of the tone burst. Rebound from inhibition then generates the off response at the termination of the tone. SPON cells then send GABAergic inhibition to the ipsilateral inferior colliculus (IC) and autaptic feedback that acts to limit the duration of the off discharge. Adapted from Kulesza R.J., Jr., Kadner, A., Berrebi, A.S. (2007) Distinct roles for glycine and GABA in shaping the response properties of neurons in the superior paraolivary nucleus of the rat. J Neurophysiol 97:1610–1620. By permission of American Physiological Society. B: Projections from auditory brainstem nuclei in Mexican free tailed bats to IC. C: Off responses recorded from SPON of rats to tones IC in Mexican free tailed bats. Adapted from Grothe, B. Schweizer, H., Pollak, G.D., Schuller, G. and Rosemann, C. (1994) Anatomy and projection patterns of the superior olivary complex in the Mexican free-tailed bat, Tadarida brasiliensis mexicana. J Comp Neurol 343:630–646. By permission of John Wiley & Sons.

Fig. 3

Two on-off cells recorded from the inferior colliculus of Mexican free-tailed bats with patch electrodes. Tone bursts were 50 dB SPL in both cells and in each cell the tones evoked an onset and offset IPSP over a wide range of frequencies. Tone burst durations are shown by the time bars. Brackets indicate the small range of mid-frequencies that evoked an onset IPSP but no offset IPSP. The midrange frequencies also evoked a depolarization that is most prominent in panel A. Data adapted from Xie, R., Gittelman, J.X. and Pollak, G.D. (2007).

Fig. 4

Responses evoked in an on-off neuron with two different tone burst durations, showing that the neuron responded with IPSPs to the onset and offset of the tone bursts. Tone bursts were 25 kHz at 50 dB SPL. Adapted from Xie, R., Gittelman, J.X. and Pollak, G.D. (2007) Rethinking tuning: in vivo whole-cell recordings of the inferior colliculus in awake bats. J Neurosci 27:9469–9481. By permission of Society for Neuroscience.

Fig. 5

Responses evoked in an on-off cell by frequency modulated (FM) signals having different durations and sweep directions. Discharges were evoked by all downward sweeping FMs regardless of duration (sweep rate) but no discharges were evoked by any upward sweeping FM. All FMs were 50 dB SPL. Adapted from Xie, R., Gittelman, J.X. and Pollak, G.D. (2007) Rethinking tuning: in vivo whole-cell recordings of the inferior colliculus in awake bats. J Neurosci 27:9469–9481. By permission of Society for Neuroscience.

Fig. 6

Intracellular responses recorded in an on-off cell from the IC of an awake bat with a patch electrode. Responses were evoked by two communication calls, a courtship chirp that had several notes that swept downward in frequency, and a dominance call composed largely of a constant frequency component. The cell discharged to the FM sweeps in the courtship call but responded to the tone-like dominance call with IPSPs at the onset and offset of the call, in a manner similar to the way on-off cells respond to tones. Both signals were 50 dB SPL (Xie and Pollak, unpublished data).

Fig. 7

Circuitry that could account for the tuning features of on-off cells in the inferior colliculus. The responses of an on-off cell evoked by 50 dB SPL tones are shown in upper left panel (same cell shown Fig. 3A). The hypothesis proposes that the onset IPSPs are evoked by glycinergic projections from the VNLLc. The broad tuning of VNLLc cells is shown in lower left (green tuning curve) and accounts for the broadly tuned onset IPSPs of on-off cells. Projections from two differently tuned SPON cells could account for the IPSPs evoked at the offset of tone bursts (blue tuning curves in lower right panel). Two differently tuned SPON cells are suggested because off IPSPs are not evoked by midrange frequencies of 23–25 kHz, but are prominent at lower frequencies, from about 13 to 21 kHz, and at higher frequencies, from about 27 to 35 kHz. A more sharply tuned excitatory input from an unknown source with a best frequency in a midrange frequency is shown in red in the lower middle panel. That excitatory input accounts for the prominent depolarizations evoked by 23–25 kHz tone bursts in the tuned region, shown with brackets in the upper left panel. The top panel shows the superposition of the proposed inputs. Note that at 50 dB SPL, the midrange frequencies should evoke an onset IPSP, due to activation of the broadly tuned VNLLc, but not offset IPSPs since those frequencies fail to excite either of the two SPON inputs. The midrange frequencies should also activate the proposed excitatory input and thus evoke depolarizations.