Inhibitory suppression of heterogeneously tuned excitation enhances spatial coding in CA1 place cells

The authors investigate the role of inhibition in shaping spatial selectivity of CA1 place cells. Combining whole-cell recordings, optogenetics and computational modeling, they demonstrate that inhibition enhances both rate and temporal coding of space by counteracting noise from broad out-of-field...

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Vydáno v:	Nature neuroscience Ročník 20; číslo 3; s. 417 - 426
Hlavní autoři:	Grienberger, Christine, Milstein, Aaron D, Bittner, Katie C, Romani, Sandro, Magee, Jeffrey C
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	New York Nature Publishing Group US 01.03.2017 Nature Publishing Group
Témata:	631/378/116/2392 631/378/1595/1554 631/378/2629/2630 631/378/3920 64 64/60 9/74 Animal Genetics and Genomics Animals Behavioral Sciences Biological Techniques Biomedicine CA1 Region, Hippocampal - physiology Electrophysiology Female Hippocampus (Brain) Interneurons - physiology Locomotion - physiology Male Membrane Potentials - physiology Mice Models, Neurological Neural Inhibition - physiology Neurobiology Neurosciences Place Cells - physiology Pyramidal Cells - physiology United States
ISSN:	1097-6256, 1546-1726
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Abstract	The authors investigate the role of inhibition in shaping spatial selectivity of CA1 place cells. Combining whole-cell recordings, optogenetics and computational modeling, they demonstrate that inhibition enhances both rate and temporal coding of space by counteracting noise from broad out-of-field excitation. Place cells in the CA1 region of the hippocampus express location-specific firing despite receiving a steady barrage of heterogeneously tuned excitatory inputs that should compromise output dynamic range and timing. We examined the role of synaptic inhibition in countering the deleterious effects of off-target excitation. Intracellular recordings in behaving mice demonstrate that bimodal excitation drives place cells, while unimodal excitation drives weaker or no spatial tuning in interneurons. Optogenetic hyperpolarization of interneurons had spatially uniform effects on place cell membrane potential dynamics, substantially reducing spatial selectivity. These data and a computational model suggest that spatially uniform inhibitory conductance enhances rate coding in place cells by suppressing out-of-field excitation and by limiting dendritic amplification. Similarly, we observed that inhibitory suppression of phasic noise generated by out-of-field excitation enhances temporal coding by expanding the range of theta phase precession. Thus, spatially uniform inhibition allows proficient and flexible coding in hippocampal CA1 by suppressing heterogeneously tuned excitation.
AbstractList	Place cells in the CA1 region of the hippocampus express location-specific firing despite receiving a steady barrage of heterogeneously tuned excitatory inputs that should compromise output dynamic range and timing. We examined the role of synaptic inhibition in countering the deleterious effects of off-target excitation. Intracellular recordings in behaving mice demonstrate that bimodal excitation drives place cells, while unimodal excitation drives weaker or no spatial tuning in interneurons. Optogenetic hyperpolarization of interneurons had spatially uniform effects on place cell membrane potential dynamics, substantially reducing spatial selectivity. These data and a computational model suggest that spatially uniform inhibitory conductance enhances rate coding in place cells by suppressing out-of-field excitation and by limiting dendritic amplification. Similarly, we observed that inhibitory suppression of phasic noise generated by out-of-field excitation enhances temporal coding by expanding the range of theta phase precession. Thus, spatially uniform inhibition allows proficient and flexible coding in hippocampal CA1 by suppressing heterogeneously tuned excitation. The authors investigate the role of inhibition in shaping spatial selectivity of CA1 place cells. Combining whole-cell recordings, optogenetics and computational modeling, they demonstrate that inhibition enhances both rate and temporal coding of space by counteracting noise from broad out-of-field excitation. Place cells in the CA1 region of the hippocampus express location-specific firing despite receiving a steady barrage of heterogeneously tuned excitatory inputs that should compromise output dynamic range and timing. We examined the role of synaptic inhibition in countering the deleterious effects of off-target excitation. Intracellular recordings in behaving mice demonstrate that bimodal excitation drives place cells, while unimodal excitation drives weaker or no spatial tuning in interneurons. Optogenetic hyperpolarization of interneurons had spatially uniform effects on place cell membrane potential dynamics, substantially reducing spatial selectivity. These data and a computational model suggest that spatially uniform inhibitory conductance enhances rate coding in place cells by suppressing out-of-field excitation and by limiting dendritic amplification. Similarly, we observed that inhibitory suppression of phasic noise generated by out-of-field excitation enhances temporal coding by expanding the range of theta phase precession. Thus, spatially uniform inhibition allows proficient and flexible coding in hippocampal CA1 by suppressing heterogeneously tuned excitation.
Audience	Academic
Author	Romani, Sandro Milstein, Aaron D Magee, Jeffrey C Grienberger, Christine Bittner, Katie C
Author_xml	– sequence: 1 givenname: Christine surname: Grienberger fullname: Grienberger, Christine organization: Howard Hughes Medical Institute, Janelia Research Campus – sequence: 2 givenname: Aaron D orcidid: 0000-0002-7186-5779 surname: Milstein fullname: Milstein, Aaron D organization: Howard Hughes Medical Institute, Janelia Research Campus – sequence: 3 givenname: Katie C surname: Bittner fullname: Bittner, Katie C organization: Howard Hughes Medical Institute, Janelia Research Campus – sequence: 4 givenname: Sandro orcidid: 0000-0002-4727-4207 surname: Romani fullname: Romani, Sandro organization: Howard Hughes Medical Institute, Janelia Research Campus – sequence: 5 givenname: Jeffrey C surname: Magee fullname: Magee, Jeffrey C email: mageej@janelia.hhmi.org organization: Howard Hughes Medical Institute, Janelia Research Campus
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/28114296$$D View this record in MEDLINE/PubMed
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Snippet	The authors investigate the role of inhibition in shaping spatial selectivity of CA1 place cells. Combining whole-cell recordings, optogenetics and... Place cells in the CA1 region of the hippocampus express location-specific firing despite receiving a steady barrage of heterogeneously tuned excitatory inputs...
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SubjectTerms	631/378/116/2392 631/378/1595/1554 631/378/2629/2630 631/378/3920 64 64/60 9/74 Animal Genetics and Genomics Animals Behavioral Sciences Biological Techniques Biomedicine CA1 Region, Hippocampal - physiology Electrophysiology Female Hippocampus (Brain) Interneurons - physiology Locomotion - physiology Male Membrane Potentials - physiology Mice Models, Neurological Neural Inhibition - physiology Neurobiology Neurosciences Place Cells - physiology Pyramidal Cells - physiology
Title	Inhibitory suppression of heterogeneously tuned excitation enhances spatial coding in CA1 place cells
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