Interneuron diversity and the cortical circuit for attention Paul Tiesinga Computational Neurophysics Lab at UNC http://neuro.physics.unc.edu Title art: from the 2005 Science and Engineering Visualization Challenge organized by Science Magazine

A “VSD” Experiment Map(s), connectivity: suppression, facilitation, biased competition, STRFs, synchrony

Input to cortex Output of cortex LGN

1. Interneurons

Interneuron diversity FFI: PV+/FS TDI CR+/CB+ Markram et al (2004) NRN

Circuit of CR+ interneurons Macaque Meskanaite, CerCor (1997) Rat

2. Stimulus competition (V4)

The model TDI TDI FFI FFI E E Column 2 Column 1

Picture from Okinawa course website

Symbols for Stimulus conditions Receptive field Neuron 2 + + Stimulus location 2 Receptive field Neuron 1 Neuron 1 Neuron 2 Pref. stimulus Nonpref. Stimulus location 1

The model (1250 synaptically-coupled single-compartment neurons with Hodgkin-Huxley-type channels) Column 1 Topdown: FEF TDI TDI 50 FFI FFI 75 Feedforward: V2 E E 500 TDI: top-down interneuron FFI: feed-forward interneuron FEF: frontal eye fields

Stimulus competition requires a switch FFI FFI E E Buia & PT,JNP 2008

3. Attention modulation (V4)

Task and so on Attend away from receptive field Attend into receptive field Salinas & Sejnowski NRN 2001

Feature attention + + + + F-att Feature attention TDI FFI E Attend the feature red (preferred feature neuron 1) + + FFI Attend the feature blue (preferred feature neuron 2) + + E

Feature attention biases competition

Response-gain like

Spatial attention + + + + TDI Spatial attention FFI S-att E Spatial attention to location 1 + + FFI + + Spatial attention to location 2 S-att E

Spatial attention biases competition

Contrast-gain like

Hypothesis Feature attention versus spatial attention Top-down (first) versus bottom-up (later) Response gain versus contrast gain

4. Back to interneurons

Contrast response surface of E-cells Stimulus competition

The FFI always increase their rate with spatial attention

With feature attention, FFI rate changes are in opposite direction to those of E-cells

5. Oscillations and synchrony

Stimulus competition is signaled by beta oscillations Stimulus onset FFI2 FFI1 E2 E1 Buia & PT,JNP 2008

In the pair condition, synchrony during feature-attention has a beta and gamma component TDI E FFI E

Beta vs Gamma TDI TDI Gamma (ING) FFI FFI Beta (PING) E E

Summary For the first time the responses at the ‘four corners’ under different attention conditions are reproduced using a single, spiking network model (Exp: many). Two types of interneurons (FFI, TDI) are needed. During spatial attention the FFI increase their rate, whereas during feature attention they decrease their rate. (Exp: Mitchel et al 2007) The TDI increase their rate with feature attention and synchronize their home column. (Exp: none) Strong competition between the two columns leads to beta oscillations, whereas feature attention leads to gamma oscillations. (Exp: Bichot et al 2005) Hypothesis: TDI are CR+ (or CB+) double bouquet cells, possibly adapting, FFI are PV+ basket cells, fast spiking.

Experimental confirmation Monkey model Task combining feature and spatial attention with same stimulus Distinguish interneurons from pyramidal cells Rabies/herpes virus based transsynaptic tracing Mice model Interneuron specific promoter coupled to fluorescent protein Two photon calcium imaging Develop behavioral task

Thanks to Calin Buia (Harvard Medical School) Amelia Cohen (UNC) Terry Sejnowski (Salk institute) Jorge Jose (SUNY Buffalo/Northeastern University)