Daniel J. Thengone , Yunguo Yu , Eyal I. Nitzany, Jonathan D. VictorBrain and Mind Research Institute, Weill Cornell Graduate School of Medical Sciences, New York, NY, 10065
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Orientation (deg)
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Adaptation-induced tuning shifts in excitatory and inhibitory neurons of the primary visual cortex
The brain employs a variety of strategies to adjust to changes in the external world. Adaptation is one such strategy, as it modifies responses based on recent inputs. As with other modulatory influences (such as attention) that affect network dynamics, adaptation is likely to involve a broad range of processes at the neuronal level. Here we study how adaptation influences neuronal responses in functionally distinct cortical cell-categories (excitatory vs inhibitory) in two hierarchically-related brain regions, V1 and V2, of the visual pathway.
We performed multi-tetrode single-unit recordings to measure neural responses to drifting sinusoidal gratings before and after 400ms adaptation to preferred and non-preferred stimuli
Based on online analysis of tuning measured at 6 tetrodes, the adapting orientations are chosen. In this example, neural activity at 3 of 6 tetrodes have peaks within 22.5 degrees of a common direction. The vertical bars (a 90 and 112.5) are therefore selectected for adaptation experiments. Stimuli are presented at the spatial frequency that is optimal for at least one of the six tetrodes.
Methods
Based on the bimodality in the distribution of trough to peak widths (p < 0.01 by the Hartigan dip test), we classified extracellular waveforms as narrow-spiking (<405μs) putative inhibitory interneurons and broad-spiking (>430μs) putative excitatory neurons (consistent with Mitchell et al., 2007 ). Neurons within 10% of the notch were labeled unclassified and not used in further analyses. For the data collected in this study the same criteria were utilized to classify the two functionally distinct cell-types.
Selection of Adaptation Parameters
Population Results
Extracellular wave shape analysis
Introduction and Motivation
Neu
ral R
espo
nse
Predicted Adaptation EffectsOFF AXISON AXISUnadapted tuning
ModelU
ntun
ed In
hibi
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hibi
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-Syn
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Adaptation at Preferred Axis
Adaptation-induced tuning shifts in models of orientaton selectivity
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Physiological methodsMacaque V1 and V2Anesthesia: sufentanil and propofolNeuromuscular blockade: rocuronium
Recordings6-tetrode array, each independently movableSpike sorting(KlustaKwik and Klusters)Lesions and histology performed post experiment
Adaptation Paradigms
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Three models for adaptation effects on orientation tuning. Arrows indicate the strength of connections from pre- to post-synaptic neurons. Row 1: postsynaptic adaptation. Adaptation reduces all connection strengths by the same factor, but no change in the tuning curve shape . Row 2: presynaptic adaptation of excitatory inputs. Adaptation modulates the connection strengths in proportion to the activity of the presynaptic neuron. Off-axis adaptation shifts the tuning curve, but only in a repulsive manner. Row 3, presynaptic adaptation and tuned inhibition: Off-axis adaptation can lead to attractive shifts in the tuning curve .
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Both brief and prolonged adaptation at the preferred axis induces changes in orientation selectivity and half-bandwidth in excitatory (blue) and inhibitory (red) cells. In most cases, tuning shifted away from the adapter (i.e a “repulsive” tuning shift).
Cortical Area V1 Granular Layer
Cortical Area V1 Supragranular Layers
Cortical Area V2
Pos
t-Ada
ptat
ion
In contrast to adaptation at the preferred axis, both brief and prolonged adaptation at a non- preferred orientation axis induces attractive shifts (towards the adapter) in excitatory and inhibitory units.
Brief adaptation induces broadening of half-bandwidth and decreases in orientation selectivity. However prolonged adaptation induces narrowing of half-bandwidth with decreases in orientation selectivity.
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For each recording site, two adaptation experiments are performed, one at 0.4sec and another at 40 sec durations. These times are chosen known to demonstrate adaptation-induced effects in V1 (Patterson et al, 2013).
Pre-Synaptic
Post-Synaptic
Site of Adaptation Type of Inhibition
Model
Tuned or Untuned
Untuned
Tuned
Gain reduction
Bandwidth NarrowingGain reduction
Bandwidth Narrowing or Broadening
Gain reduction
Less gain reduction; No Orientation Shifts
Less gain reduction; Bandwidth Narrowing;Repulsive shifts only
Less gain reduction; Bandwidth Narrowing;Attractive or Repulsive shifts
Predicted Adaptation Effects
Adaptation NonPreferred AxisAdaptation Preferred Axis
Half-Bandwidth Orientation Selectivity Half-Bandwidth Orientation Selectivity
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In area V2, adaptation at the preferred axis induces both broadening and narrowing of half-bandwidth in the inhibitory units, while the excitatory units mostly narrow their half-bandwidths and increase their orientation selectivity. Orientation tuning in the two cell types mostly shifts away from the adapter with brief or prolonged stimulation.
Adaptation at Non-Preferred Axis
Both attractive and repulsive shifts with brief and prolonged stimulation, are observed in V2, similar to visual cortical area V1.
Tuning Shifts
Tuning Shifts
Brief Adaptation
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pTe
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pTe
stBlan
kProlonged Adaptation
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Time (sec)
Adaptation at NonPreferred Axis
Adaptation at Preferred AxisHalf-Bandwidth Orientation Selectivity
Adaptation at Preferred AxisHalf-Bandwidth Orientation Selectivity
Brief Prolonged
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Orientation tuning shift Orientation tuning shift
V1 V2
SummaryExcitatory and inhibitory neurons both show adaptive shifts of their orientation tuning curves, for brief and prolonged presentations of the adapting stimulus.
In the supragranular layer of V1, adaptation to non-preferred orientations induces strong attractive shifts (towards the adapter), in contrast to adaptation at the preferred axis.
In the granular layer of V1, prelimiary evidence suggest that brief adaptation at the preferred axis induces mostly broadening of the half-bandwidth, while prolonged adaptation induces predominantly narrowing of the half-bandwidth
In visual cortical area V2, adaptation induces mostly narrowing of orientation tuning in excitatory cells, but tends to increase or decrease the inhibitory interneurons based on their selectivity at baseline. Both repulsive and attractive shifts in tuning are observed in the two cell types with adaptation.
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Tuning shifts
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1. Abbott, L. F., Varela, J. A., Sen, K., & Nelson, S. B. (1997). Synaptic depression and cortical gain control. Science, 275(5297), 221-224.2. Dragoi, V., & Sur, M. (2004). Plasticity of orientation processing in adult visual cortex. Visual Neurosciences, 1654-1664.3. Kohn, A. (2007). Visual adaptation: physiology, mechanisms, and functional benefits. Journal of neurophysiology, 97(5), 3155-3164. 4. Mitchell, J. F., Sundberg, K. A., & Reynolds, J. H. (2007). Differential attention-dependent response modulation across cell classes in macaque visual area V4. Neuron, 55(1), 131-141.5. Patterson, C. A., Wissig, S. C., & Kohn, A. (2013). Distinct effects of brief and prolonged adaptation on orientation tuning in primary visual cortex. The Journal of Neuroscience, 33(2), 532-543.6. Shapley, R., Hawken, M., & Ringach, D. L. (2003). Dynamics of orientation selectivity in the primary visual cortex and the importance of cortical inhibition. Neuron, 38(5), 689-699.
References
Support: NIH EY09314
contact: [email protected]
Orientation tuning shift
Orientation tuning shift Orientation tuning shift
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