The role of thalamic synchrony in gating information flow to cortex A ubiquitous property of sensory pathways is that they continuously adapt to changes in the properties of the sensory input. Adaptation is not simply fatigue or attenuation of neural activity, but instead can fundamentally change the features to which the sensory pathway are sensitive and thus changes what the pathway encodes. We have recently shown that adaptation through ongoing tactile stimulation in the rat vibrissa system induces a fundamental change in what behaviorally relevant features the cortex encodes: from detection of a tactile contact to discrimination between different speeds of the tactile/whisker input. To what extent this observation is general and whether it manifests perceptually has not been well studied. In this project, using a combination of electrophysiology and related functional measures and behavior, we will determine whether adaptation enhances discrimination at the expense of detection through modulation of the timing synchrony of thalamic input to cortex. We do so through an integrated, parallel study using multiple recording techniques in the vibrissa pathway of the anesthetized rat, and using behavioral tasks focused on detection of and discrimination between tactile stimuli. Specifically, we will test whether adaptation switches the fundamental cortical processing mode from detection to discrimination through modulation of synchrony of projecting thalamic input (AIM 1). We will directly test the generality of this central hypothesis across whisker deflection speed and direction, and in the context of spatial acuity across whiskers, and determine how this phenomenon is shaped by the statistics of the adapting tactile input. Second, we will directly test whether adaptation switches perceptual performance from detector to discriminator during behavior and whether modulation of thalamic synchrony mediates the switch (AIM 2). Rats will be trained to either detect whisker contact or discriminate between contacts of nearby whiskers, while we monitor population activity in VPm thalamus through chronically implanted multi-electrodes within and across vibrissa-specific regions. Significance: It has long been posited that adaptation acts to enhance information flow in sensory pathways and human psychophysical studies have indeed shown that in certain circumstances adaptation acts to enhance discriminability of tactile inputs. However, the precise link between the underlying neural representations in the thalamocortical circuit and the resultant percept remains a major open question in neuroscience. Success of our aims will directly determine how the cortical representation changes through modulation in thalamic input and the consequences of this on perception. Broad Impacts: Various brain pathologies such as autism, concussive injuries, and alcoholism result in an impaired effect of adaptation on spatial acuity. Success of our aims will provide a more solid foundation for sensory-based diagnostics, and may help to shed light on the pathophysiology associated with these life-altering disorders. Further, one mechanism that we explore is that of thalamic synchrony and its effect on cortical activation, which has been implicated in seizure generation and thalamic pain.

Public Health Relevance

Sensory input is critical in our daily lives, for both the perception of the world around us, and in providing feedback for our muscle systems that help us interact with the external world. How the nervous system performs this feat, and precisely how this helps us in our environment, is unknown. Discovery in this area can potentially help us understand a number of disorders/diseases of the nervous system for which individuals exhibit loss of acuity/sensitivity, and do not have the ability to adapt to changes in the sensory environment.

Agency
National Institute of Health (NIH)
Institute
National Institute of Neurological Disorders and Stroke (NINDS)
Type
Research Project (R01)
Project #
5R01NS048285-08
Application #
8534819
Study Section
Sensorimotor Integration Study Section (SMI)
Program Officer
Gnadt, James W
Project Start
2004-01-01
Project End
2015-08-31
Budget Start
2013-09-01
Budget End
2014-08-31
Support Year
8
Fiscal Year
2013
Total Cost
$302,437
Indirect Cost
$91,343
Name
Georgia Institute of Technology
Department
Engineering (All Types)
Type
Schools of Engineering
DUNS #
097394084
City
Atlanta
State
GA
Country
United States
Zip Code
30332
Kelly, Sean T; Kremkow, Jens; Jin, Jianzhong et al. (2014) The role of thalamic population synchrony in the emergence of cortical feature selectivity. PLoS Comput Biol 10:e1003418
Ollerenshaw, Douglas R; Zheng, He J V; Millard, Daniel C et al. (2014) The adaptive trade-off between detection and discrimination in cortical representations and behavior. Neuron 81:1152-64
Millard, Daniel C; Wang, Qi; Gollnick, Clare A et al. (2013) System identification of the nonlinear dynamics in the thalamocortical circuit in response to patterned thalamic microstimulation in vivo. J Neural Eng 10:066011
Stanley, Garrett B (2013) Reading and writing the neural code. Nat Neurosci 16:259-63
Wang, Qi; Millard, Daniel C; Zheng, He J V et al. (2012) Voltage-sensitive dye imaging reveals improved topographic activation of cortex in response to manipulation of thalamic microstimulation parameters. J Neural Eng 9:026008
Ding, Ming-Chieh; Wang, Qi; Lo, Eng H et al. (2011) Cortical excitation and inhibition following focal traumatic brain injury. J Neurosci 31:14085-94
Boloori, Ali-Reza; Jenks, Robert A; Desbordes, Gaelle et al. (2010) Encoding and decoding cortical representations of tactile features in the vibrissa system. J Neurosci 30:9990-10005
Wang, Qi; Webber, Roxanna M; Stanley, Garrett B (2010) Thalamic synchrony and the adaptive gating of information flow to cortex. Nat Neurosci 13:1534-41
Jenks, Robert A; Vaziri, Ashkan; Boloori, Ali-Reza et al. (2010) Self-motion and the shaping of sensory signals. J Neurophysiol 103:2195-207
Ding, M C; Lo, E H; Stanley, G B (2008) Sustained focal cortical compression reduces electrically-induced seizure threshold. Neuroscience 154:551-5

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