Data courtesy: Alex Goddard

Gamma-band spike-field coherence in the optic tectum of the barn owlSridharan Devarajan, Kwabena Boahen, Eric Knudsen

Departments of Neurobiology and Bioengineering, Stanford University

• J. V. Arthur, K. A. Boahen, IEEE Trans. Neural Netw. 18, 1815 (2007).

• H. Luksch, Rev. Neurosci. 14, 85 (2003). • J. R. Muller, M. G. Philiastides, W. T. Newsome, Proc.

Natl. Acad. Sci. U. S. A. 102, 524 (2005).• T. Williford, J. H. R. Maunsell, J. Neurophysiol. 96,

40 (2006).

Literature Cited

Maintenance of a “goal” in working memory (e.g. distinguishing food from dirt)

The Imc circuit is well-placed to suppress the representation of distractors (red).

Attention

Stimulus selection in the optic tectum

Orienting to salient stimuli in the environment (e.g. sudden appearance of a predator)

Enhanced firing rate, and sharpened receptive field (RF)

Summary

Previous models have attempted to link these two signatures of attention, but have ignored the underlying neural circuitry.

Synchronization among neuronal spikes is known to be an important signature of target selection in primates. Little is known, however, about the cellular and network mechanisms underlying the induction of this synchrony.

Using recordings of single neurons and local field potentials in the optic tectum of the barn owl (Tyto alba), we find that gamma-synchrony is a signature of stimulus selection and distractor suppression.

By modeling the tectal circuit in-silico, on neuromorphic hardware, we show that mimicking the effects of neuromodulation by acetylcholine is a potential mechanism for evoking synchrony during bottom-up stimulus selection.

Neuronal signatures

Reduced threshold and increased sensitivity

Network signatures

Spikes synchronize and phase lock with LFP

LFP shows strong gamma

(γ) rhythm (30-90Hz)

Here we focus on the neural mechanisms of bottom-up stimulus selection, a fundamental component of attention.

Isthmotectal microcircuit

Being part of the avian gaze control circuitry, the optic tectum (OT) is ideally suited for stimulus selection. Its homolog in primates (superior colliculus, SC) is known to contribute importantly to spatial attention (Muller et al, 2005).

Target Enhancement Distractor Suppression

The Ipc circuit is well-placed to enhance the representation of target stimuli.

The cholinergic Ipc circuit, and the GABA-ergic Imc circuit can be engaged by bottom-up inputs from the retina or top-down inputs from the forebrain gaze fields (AGF), thereby initiating or suppressing motor output.

Stimulus evoked gamma-band LFP

We model a single column in OT with spatially localized RF on a neuromorphic chip with 1024 excitatory and 256 inhibitory neurons.

Modeling the circuit in-silico

NeuronChip

Arthur & Boahen, 2007

Ipc (green, biocytin) projects homotopically to the optic tectum (arrow, insert), terminating in layer 5, rich with inhibitory neurons (red, calbindin). These interneurons have widespread horizontal arbors. Excitatory cells (blue, DAPI) in layers 8-10 also send their dendrites up into layer 5.

Retinal axons synapse onto both excitatory and inhibitory neurons in layers 1-5 (Luksch, 2003).

Detailed isthmotectal neuroanatomy

4x

40x

Image courtesy: Alex Goddard

Image courtesy: Phyllis Knudsen

Key Predictions and Future directions

ACh input from Ipc to OT facilitates fast excitatory (AMPA) synapses from the retina onto both excitatory (E) and inhibitory

(I) neurons.

Contrast response function shifts right (less sensitivity)

Gamma-synchrony reduces (if not eliminated)

We hypothesize that neuronal and network signature of attention are linked by ACh neuromodulation

This hypothesis predicts that inactivating the Ipc (ACh nucleus) should disrupt both neural and network signatures:

Future work will involve testing the key predictions of the model by inactivating the Ipc, while recording in the OT (in-vivo), as well as microstimulating Ipc (in-vitro) to test if ACh input to OT can induce synchrony. The transient increase in synchrony upon stimulus offset will be incorporated into a revised model.

AcknowledgmentsThis work was supported by grants NIH1 R01-DC00155-25 (EK) and the NIH Director’s Pioneer Award Program Grant DPI-OD000965 (KB). SD wishes to thank John Arthur for his help with programming the chip, and Alex Goddard and Phyllis Knudsen for kindly sharing images. Spectral analyses were performed with the Chronux toolbox (www.chronux.org)

Data courtesy: Alex Goddard

Contrast response

Spatial tuning

Neuronal signature Network signature

In collab. with: Shreesh Mysore

Facilitation of excitation Facilitation of inhibition

E

Retina

ACh

L-8

RetinaACh

L-8

I L-4

E

Layer 4/5

Layer 8/10

Optic Tectum

AMPA (excitatory)

GABA (inhibitory)

ACh (cholinergic)

Synapses

Retina

Ipc

E

Imc

II

Inhibitory

Excitatory

Neurons

I

E

Gaze Control

In-vivo

In-silico

?

LFP spectrogram

LFP spectrogram

Spatial tuning Contrast response