Introduction

ATTENTION SPANS MULTIPLE STIMULUS DIMENSIONS IN MACAQUE VISUAL CORTEX Jitendra Sharma*, James Schummers, Hiroki Sugihara, Paymon Hosseini and Mriganka Sur

Picower Center for Learning and Memory, Department of Brain and Cognitive Sciences, MIT, Cambridge, MA 02139

Summary

411.2

Background

Visuo-spatial attention involves a two way process of enhancing perception of the attended stimulus while inhibiting non-attended stimuli. Attentional modulations have been likened to contrast gain mechanisms that serve to bias competitive interactions between multiple stimuli towards the attended stimulus. However, the locus and mechanism underlying such biased processing remains unresolved. Furthermore, most previous studies on attention have shown that there occurs a simple increase in neuronal firing rate to the attended stimulus. It however remains unclear if particular characteristics of stimulus such as size, orientation, contrast or spatial frequency of engage greater or less attention and whether such a change dynamically modify spatial and temporal dimensions of neuronal responses. In this study we simultaneously recorded neuronal responses in V1 and V4 in awake behaving monkeys to a dynamically changing stimulus pattern that overlapped receptive fields (RF) of single neurons in both areas. The monkeys were trained in a covert spatial attention task where monkeys passively attended towards or away from the RF continuously for the entire period of the trial. We used a reverse correlation paradigm to study the dynamics of attentional modulation for different stimulus dimensions.

Methods:

Behavioral Task: Monkeys were trained to covertly attend to a small attention spot that could appear towards the RF on the recorded neurons or away from it, in a contralateral location. The task sequence started with monkey holding a lever that brought a red fixation spot (0.1 deg.). They were required to hold fixation within a small window such that any jitter in fixation > 0.25 deg. aborted the trial. Once the monkey acquired stable fixation, an attention spot and an equiluminant distracter were simultaneously presented towards the RF or in the contralateral hemifield. Monkeys were required to hold fixation release the lever within 350-400ms of the disappearance of the attention spot. The attention spot could appear towards the RF (attend Towards) or away from the RF (attend Away) in a random order. To prevent monkeys from anticipating attention spot disappearance, the trials could last in time windows of 600ms, 1200 ms and 1800 ms, and within each window there was a further randomization of up to 500 ms. This made the task attentionally demanding.

Behavioral Control & Recording: The behavioral task and stimulus presentation was controlled by CORTEX (NIMH freeware). Extracellular unit recordings were done in V1 and V4 from neurons having receptive fields centers within 6° from the center of gaze. Before commencing the recording, RF size, location and other characteristics were carefully mapped to optimize stimulus location. Spike sorting and post processing were done using custom software written in Matlab.

ResultsComplex dynamics in V4 enhanced by surround stimulus

Cell A (V4)

000 90

Orientation (°)

900

154

126

98

Tim

e (m

sec)

70

42

1450 100

90

0

50 100

Time (msec.)

Orie

ntat

ion

(°)

00 90

Orientation (°)

900

154

126

98

Tim

e (m

sec)

70

42

1450 100

90

0

50 100

Time (msec.)

Orie

ntat

ion

(°)

Cell B (V4)Attention Towards

Attention Away

Attention Towards

Attention Away

3.

1) Spatial attention to the receptive field location leads to increased coarse firing rate in response to dynamic grating stimulus movies

2) Time course of this effect includes both early and late components in V4 neurons, but only late component in V1 neurons

3) Temporal dynamics in V4 neurons depend on stimulus configuration; surround stimuli largely suppress responses, and in some cases lead to “mexican hat” tuning

4) Surround suppression in V1 is preceded by facilitatory responses.

5) This is the first report of reverse-correlation analysis of temporal dynamics underlying behavioral effects

Stimulus

Spike Train

Time

~13 msec

RF

…

…

…

t2= t1+ 600/1200/1800ms (randomized)

400 ms

Fixation

Attention Cue

Stimulus on

Attention cue off

Reward

Attention spot

Distractor

CRF

Time = t

t1= t+300ms

t3= t2+500ms (randomized)

Fix-spot

Stimulus

time

Response(Bar Release)

Bar Press

Stimulus

Stimuli: The stimulus consisted of patches of gray sinusoidal gratings consisting of 8 orientations, two different sizes (2° and 5° for V1 neurons and 4° and 8° for V4 neurons) and two contrasts of 20% and 60%. Spatial frequencies were optimized for V1 and V4 neurons (typically 3 cycles /deg and 0.5 cycles / deg. respectively). Each stimulus frame was presented in rapid sequence at the monitor refresh rate (75 Hz) and lasted from 1100-2300 ms. There were a total of 360 conditions that were presented in a pseudo-random order. Identical patterns of stimuli were presented covering the RF and in the contralateral location. The attention spot and distracter locations were randomly chosen at two points just outside the RF so as to obviate any anticipation bias for a particular location around the RF.

Data Analysis: Responses to individual frames in the stimulus were assessed with the reverse-correlation technique. For each time delay (tau) from 0-200msec, the probability distribution of stimulus frames presented “tau” msec before a spike was calculated. The response to the blank stimulus frames was subtracted from the response to each stimulus. Orientation tuning curves were then calculated for each “tau” under four conditions consisting of two attention states: towards or away from the RF, and stimulus size: small or large.

Attention modulates firing rate response to dynamic grating stimuli1.

Time (msec)

V4 (n = 22)

-250 0 500 1000 1500 2000

10

15

20Attention Towards

Attention Away

Fir

ing

Rat

e (H

z)

Time (msec)

V1 (n = 25)

-250 0 500 1000 1500 2000

20

25

30

Attention Towards

Attention Away

0

2

4

6

Mean = 0.06* Mean = -0.01 Mean = 0.05*

-0.2 0 0.2 -0.2 0 0.2 -0.2 0 0.2 -0.2 0 0.2

Mean = 0.06*

0

5

10Mean = -0.01 Mean = 0.025** Mean = 0.05**

-0.2 0 0.2 -0.2 0 0.2 -0.2

0 0.2 -0.2 0 0.2

Mean = 0.06**

Top: Population average PSTH representation of responses to the dynamic grating stimulus for V4 neurons (left) and V1 neurons (right), under two behavioral conditions: attention towards the RF, or away from the RF. In both visual areas, attention to the RF increases the firing rate, compared to the attention away condition. Bottom: Histograms of the Modulation Index (MI) of the firing rate ([FRtow-FRawy]/[FRtow+FRawy]) for four different epochs during the stimulus presentation (250-750, 750-1350, 1350-1950 and 1950-1550 msec). During the later epochs, there is a strong trend for cells to shift to higher MI values, indicating an increase in response for attend towards condition. (* = p<0.1; ** = p<0.05)

1 2 43 1 2 43

1 2 3 4 1 2 3 4

# C

ells

Modulation Index Modulation Index

2.

V1 (n = 25)

Small Large

Towards

Away

Time

Orientation

V4 (n = 22)

Small Large

Towards

Away

Population average dynamic tuning curves

TimeOrientation

-0.5 0 0.5 -0.5 0 0.5

Population average tuning curve vs. time plots for V4 neurons (left) and V1 neurons (right). Each of the four stimulus/behavioral conditions is plotted independently. The top row contains tuning curves for the attend toward condition, and the bottom row for attend away. The stimulus size is indicated at the bottom of each column. V1 neurons are more sharply tuned for the large stimulus where excitation is followed by a prolonged suppression, V4 neurons on the other hand show an early short excitatory response followed by a sharp suppression by the large stimulus.

4. Time course of suppression in V1 and V4

Small

Large

Small

Large

V1 (n = 25)V4 (n = 22)

0 40 80 120 160 200

0.007

0.008

0.009

0.01

0 40 80 120 160 200 0 40 80 120 160 200

Time (msec.) Time (msec.)

0.01

0.02

0 40 80 120 160 200

Time (msec.) Time (msec.)

Nor

mal

ized

Pro

babi

lity

Example V4 cells showing complex temporal dynamics, related to stimulus size. Both cells exhibit simple dynamics in response to the small stimulus size (thick lines). In response to the large stimulus, however, there is dominant suppression, which results in “Mexican Hat” shaped tuning curves.

Attention Towards

Attention Away

Small

Large

Population average response dynamics. Each plot shows the average time course of response across cells, and across stimulus orientation. V4 neurons show positive-going responses for small stimulus size, but the response is almost entirely suppressive for large stimuli. In V1 neurons, the large stimuli result in larger, tuned responses.