Differential roles of GABAergic and glycinergic input on FM selectivity in the inferior colliculus of the pallid bat

Williams, Anthony; Fuzessery, Zoltan M.

doi:10.1152/jn.00569.2011

Cited by 12 publications

(18 citation statements)

References 61 publications

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“…In these cells, for the preferred sweep direction excitation precedes inhibition, whereas for the other direction inhibition coincides with excitation. It is still debated whether this mechanism can entirely explain FM direction selectivity within the inferior colliculus, or whether there is an additional role for upstream processing or the timing of excitatory inputs (Suga, 1965; Clopton and Winfield, 1974; Poon et al, 1992; Felsheim and Ostwald, 1996; Gittelman et al, 2009; Williams and Fuzessery, 2011; Kuo and Wu, 2012). …”

Section: Introductionmentioning

confidence: 99%

“…Selectivity for the rate of FM sweeps can also be created by the spectrotemporal interaction of inhibitory and excitatory inputs, but additional mechanisms are thought to play a role as well (Gordon and O'Neill, 1998; Fuzessery et al, 2006; Williams and Fuzessery, 2011, 2012). Much of the rate selectivity of inferior colliculus neurons appears to be already present in their synaptic inputs (Williams and Fuzessery, 2010, 2011; Gittelman and Li, 2011).…”

Section: Introductionmentioning

confidence: 99%

“…Much of the rate selectivity of inferior colliculus neurons appears to be already present in their synaptic inputs (Williams and Fuzessery, 2010, 2011; Gittelman and Li, 2011). …”

Section: Introductionmentioning

confidence: 99%

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Intracellular responses to frequency modulated tones in the dorsal cortex of the mouse inferior colliculus

Geis¹,

Borst²

2013

Front. Neural Circuits

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Frequency modulations occur in many natural sounds, including vocalizations. The neuronal response to frequency modulated (FM) stimuli has been studied extensively in different brain areas, with an emphasis on the auditory cortex and the central nucleus of the inferior colliculus. Here, we measured the responses to FM sweeps in whole-cell recordings from neurons in the dorsal cortex of the mouse inferior colliculus. Both up- and downward logarithmic FM sweeps were presented at two different speeds to both the ipsi- and the contralateral ear. Based on the number of action potentials that were fired, between 10 and 24% of cells were selective for rate or direction of the FM sweeps. A somewhat lower percentage of cells, 6–21%, showed selectivity based on EPSP size. To study the mechanisms underlying the generation of FM selectivity, we compared FM responses with responses to simple tones in the same cells. We found that if pairs of neurons responded in a similar way to simple tones, they generally also responded in a similar way to FM sweeps. Further evidence that FM selectivity can be generated within the dorsal cortex was obtained by reconstructing FM sweeps from the response to simple tones using three different models. In about half of the direction selective neurons the selectivity was generated by spectrally asymmetric synaptic inhibition. In addition, evidence for direction selectivity based on the timing of excitatory responses was also obtained in some cells. No clear evidence for the local generation of rate selectivity was obtained. We conclude that FM direction selectivity can be generated within the dorsal cortex of the mouse inferior colliculus by multiple mechanisms.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Intracellular responses to frequency modulated tones in the dorsal cortex of the mouse inferior colliculus

Geis¹,

Borst²

2013

Front. Neural Circuits

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“…Synaptic inhibition in the auditory system shapes spectral, temporal, and spatial selectivity properties of in vivo soundevoked responses to simple and complex sounds (Chang et al 2005;D'Angelo et al 2005;LeBeau et al 2001;Razak and Fuzessery 2009;Wang et al 2002;Williams and Fuzessery 2011). Developmental studies in the superior olivary and lateral lemniscal nuclei have shown that inhibitory synaptic properties generally become faster and more precise with age, with each auditory synapse following a unique developmental timetable (Ammer et al 2012;Awatramani et al 2005;Chirila et al 2007;Kapfer et al 2002;Magnusson et al 2005;Noh et al 2010;Walcher et al 2011).…”

mentioning

confidence: 99%

Postnatal development of synaptic properties of the GABAergic projection from the inferior colliculus to the auditory thalamus

Venkataraman

Bartlett

2013

Journal of Neurophysiology

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“…All data were recorded from the high-frequency region of the pallid bat IC (best frequency = 30–60 kHz) at penetration depths of 1000–2000 μm from the surface of the brain using a similar recording protocol as described previously (Razak and Fuzessery, 2009; Williams and Fuzessery, 2011). …”

Section: Methodsmentioning

confidence: 99%

Multiple mechanisms shape FM sweep rate selectivity: complementary or redundant?

Williams¹,

Fuzessery²

2012

Front. Neural Circuits

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Auditory neurons in the inferior colliculus (IC) of the pallid bat have highly rate selective responses to downward frequency modulated (FM) sweeps attributable to the spectrotemporal pattern of their echolocation call (a brief FM pulse). Several mechanisms are known to shape FM rate selectivity within the pallid bat IC. Here we explore how two mechanisms, stimulus duration and high-frequency inhibition (HFI), can interact to shape FM rate selectivity within the same neuron. Results from extracellular recordings indicated that a derived duration-rate function (based on tonal response) was highly predictive of the shape of the FM rate response. Longpass duration selectivity for tones was predictive of slowpass rate selectivity for FM sweeps, both of which required long stimulus durations and remained intact following iontophoretic blockade of inhibitory input. Bandpass duration selectivity for tones, sensitive to only a narrow range of tone durations, was predictive of bandpass rate selectivity for FM sweeps. Conversion of the tone duration response from bandpass to longpass after blocking inhibition was coincident with a change in FM rate selectivity from bandpass to slowpass indicating an active inhibitory component to the formation of bandpass selectivity. Independent of the effect of duration tuning on FM rate selectivity, the presence of HFI acted as a fastpass FM rate filter by suppressing slow FM sweep rates. In cases where both mechanisms were present, both had to be eliminated, by removing inhibition, before bandpass FM rate selectivity was affected. It is unknown why the auditory system utilizes multiple mechanisms capable of shaping identical forms of FM rate selectivity though it may represent distinct but convergent modes of neural signaling directed at shaping response selectivity for important biologically relevant sounds.

show abstract

Differential roles of GABAergic and glycinergic input on FM selectivity in the inferior colliculus of the pallid bat

Cited by 12 publications

References 61 publications

Intracellular responses to frequency modulated tones in the dorsal cortex of the mouse inferior colliculus

Intracellular responses to frequency modulated tones in the dorsal cortex of the mouse inferior colliculus

Postnatal development of synaptic properties of the GABAergic projection from the inferior colliculus to the auditory thalamus

Multiple mechanisms shape FM sweep rate selectivity: complementary or redundant?

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