Ageing‐related changes in GABAergic inhibition in mouse auditory cortex, measured using <i>in vitro</i> flavoprotein autofluorescence imaging

Stebbings, Kevin A.; Choi, Hyun Woo; Ravindra, Aditya; Caspary, Donald M.; Turner, Jeremy G.; Llano, Daniel A.

doi:10.1113/jp271221

Cited by 34 publications

(49 citation statements)

References 76 publications

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“…Declines in the function of inhibitory circuits in the auditory cortex, which is mostly mediated by GABAergic interneurons through feed-forward or feedback connections, have been documented in detail in aging animal models (4,23,24,(51)(52)(53). These major types of GABAergic interneurons expressing PV and SOM are argued to contribute to cortical signal representation, local and system coordination, and experience-dependent plasticity (14,18,22,(54)(55)(56)(57).…”

Section: Discussionmentioning

confidence: 99%

Positive impacts of early auditory training on cortical processing at an older age

Cheng

Jia

Zhang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Progressive negative behavioral changes in normal aging are paralleled by a complex series of physical and functional declines expressed in the cerebral cortex. In studies conducted in the auditory domain, these degrading physical and functional cortical changes have been shown to be broadly reversed by intensive progressive training that improves the spectral and temporal resolution of acoustic inputs and suppresses behavioral distractors. Here we found older rats that were intensively trained on an attentionally demanding modulation-rate recognition task in young adulthood substantially retained training-driven improvements in temporal rate discrimination abilities over a subsequent 18-mo epoch-that is, forward into their older age. In parallel, this young-adult auditory training enduringly enhanced temporal and spectral information processing in their primary auditory cortices (A1). Substantially greater numbers of parvalbumin-and somatostatin-labeled inhibitory neurons (closer to the numbers recorded in young vigorous adults) were recorded in the A1 and hippocampus in old trained versus untrained age-matched rats. These results show that a simple form of training in young adulthood in this rat model enduringly delays the otherwise expected deterioration of the physical status and functional operations of the auditory nervous system, with evident training impacts generalized to the hippocampus.aging | auditory cortex | behavioral training | cortical processing | inhibition A degradation of the status of physical brain machinery, expressed by a decline in its temporal processing abilities, has been repeatedly associated with its deteriorating functional status in normal aging (1-4). Recent studies have shown that the machinery that supports processing accuracy and speed, as well as the processes supporting attention control and distractor suppression, can be substantially rejuvenated via simple forms of intensive training in the aged-rat model (4, 5). With auditory perceptual training, in parallel with recovery in behavioral abilities to that matching young-animal performance levels, serials of key physical, chemical, and functional aspects of cortical processing machinery in the trained rats were shown to be restored to a physical or functional status that approached that normally recorded in vigorous young-adult animals.In human studies, substantial changes in speed of processing (SOP) and in other spectro-temporal (or spatiotemporal) signal resolution of performance abilities have been shown to result from attention-demanding, speed-challenged auditory (3, 5-7) or visual training (8-11). For example, the accurate behavioral identification and stimulus-order reconstruction of rapidly successive auditory stimuli was restored in human individuals trained in their eighth decade of life to a performance level normally typifying human performance abilities recorded in their third or fourth decade (3, 6).Our goal here was to define the magnitude and endurance of an intense dose of attention-demanding modulation di...

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Section: Discussionmentioning

confidence: 99%

Positive impacts of early auditory training on cortical processing at an older age

Cheng

Jia

Zhang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…The electrical parameters meet the lowest duty cycle that is required for the clearance of free radicals produced by electrical stimulation as reported in Varela, et al review [9]. In addition, this electrical paradigm generates consistent FAD signals as shown previously [97,57,96]. The parameters of the electrical pulses were adjusted by a B&K precision wave generator (model # 4063) and World Precision Instruments stimulation isolator (A-360).…”

Section: Methodsmentioning

confidence: 90%

“…Endogenous FAD and NADH signals were used to track neuronal activity in the auditory cortex after electrically stimulating the subcortical white matter in auditory thalamocortical slices [97,57,15]. Here, sending electric stimulation, to the white matter evoked synaptic activity in the auditory cortex which was associated with an increase of the FAD signal (Figure 1A).…”

Section: Resultsmentioning

confidence: 99%

“…Redox ratio is an established marker for the metabolic state of different tissue types including brain [97,65,25,90]. To determine if the temperature-dependent changes in FAD signals and neurometabolic signals described above were related to changes in resting redox state, both raw FAD and NADH endogenous fluorescence signals of brain slices were measured at different temperatures.…”

Section: Resultsmentioning

confidence: 99%

“…From the first group of mice, 600 μm thick auditory thalamocortical brain slices were obtained [15,97]. For the second group of mice guided by Allen brain atlas (http://www.brain-map.org/), 500 μm coronal slices were obtained at (+1.145 to −0.18 mm) from bregma to examine FAD and LFP signals of the spontaneous activity of layer 2/3 of the motor cortex.…”

Section: Methodsmentioning

confidence: 99%

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Effect of temperature on FAD and NADH-derived signals and neurometabolic coupling in the mouse auditory and motor cortex

Ibrahim

Wang

Lesicko

et al. 2017

Pflugers Arch - Eur J Physiol

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Tight coupling of neuronal metabolism to synaptic activity is critical to ensure that the supply of metabolic substrates meets the demands of neuronal signaling. Given the impact of temperature on metabolism, and the wide fluctuations of brain temperature observed during clinical hypothermia, we examined the effect of temperature on neurometabolic coupling. Intrinsic fluorescence signals of the oxidized form of flavin adenine dinucleotide (FAD) and the reduced form of nicotinamide adenine dinucleotide (NADH), and their ratios, were measured to assess neural metabolic state and local field potentials were recorded to measure synaptic activity in the mouse brain. Brain slice preparations were used to remove the potential impacts of blood flow. Tight coupling between metabolic signals and local field potential amplitudes was observed at a range of temperatures below 29°C. However, above 29 °C, the metabolic and synaptic signatures diverged such that FAD signals were diminished, but local field potentials retained their amplitude. It was also observed that the declines in the FAD signals seen at high temperatures (and hence the decoupling between synaptic and metabolic events), is driven by low FAD availability at high temperatures. These data suggest that neurometabolic coupling, thought to be critical for ensuring the metabolic health of the brain, may show temperature dependence, and is related to temperature-dependent changes in FAD supplies.

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Auditory temporal acuity improves with age in the male mouse auditory thalamus: A role for perineuronal nets?

Quraishe

Newman

Anderson³

2019

J of Neuroscience Research

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The ability to perceive and interpret environmental sound accurately is conserved across many species and is fundamental for understanding communication via vocalizations. Auditory acuity and temporally controlled neuronal firing underpin this ability. Deterioration in neuronal firing precision likely contributes to poorer hearing performance, yet the role of neural processing by key nuclei in the central auditory pathways is not fully understood. Here, we record from the auditory thalamus (medial geniculate body [MGB]) of young and middle‐aged, normally hearing male CBA/Ca mice. We report changes in temporal processing of auditory stimuli, with neurons recorded from ventral and medial MGB subdivisions of older animals more likely to synchronize to rapid temporally varying stimuli. MGB subdivisions also showed increased probability of neuronal firing and shorter response latencies to clicks in older animals. Histological investigation of neuronal extracellular specializations, perineuronal nets (PNNs) and axonal coats, in the MGB identified greater organization of PNNs around MGB neurons and the presence of axonal coats within older animals. This supports the observation that neural responses recorded from ventral and medial MGB of older mice were more likely to synchronize to temporally varying stimuli presented at faster repetition rates than those recorded from young adult animals. These changes are observed in animals with normal hearing thresholds, confirming that neural processing differs between the MGB subdivisions and such processing is associated with age‐related changes to PNNs. Understanding these age‐related changes and how they occur have important implications for the design of effective therapeutic interventions to improve speech intelligibility into later life.

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Ageing‐related changes in GABAergic inhibition in mouse auditory cortex, measured using in vitro flavoprotein autofluorescence imaging

Cited by 34 publications

References 76 publications

Positive impacts of early auditory training on cortical processing at an older age

Positive impacts of early auditory training on cortical processing at an older age

Effect of temperature on FAD and NADH-derived signals and neurometabolic coupling in the mouse auditory and motor cortex

Auditory temporal acuity improves with age in the male mouse auditory thalamus: A role for perineuronal nets?

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