Face recognition as a function of social attention in non-human primates: an ERP study

COGNITIVE BRAIN RESEARCH ELSEVIER

Cognitive

Brain Research

Research

2 (1994) l-12

Report

Face recognition as a function of social attention in non-human primates: an ERP study Jaime A. Pineda Department

*, Gillian Sebestyen,

of Cognitir,e Science 0515, Unir~ersir):of Cakforniu, Accepted

28 December

Carlos Nava

San Diego, La Jolla, CA 9209.W53.5, USA 1993

Abstract Elpidural event related potentials (ERPs) were recorded from four squirrel monkeys (Saimiri sciureus) during the presentation of pictoral stimuli that comprised real human and monkey faces. Subjects viewed tachistoscopically presented stimuli belonging to four different categories: familiar and unfamiliar human faces, and familiar and unfamiliar monkey faces. Familiar faces were subcategorized into top, middle and bottom according to the perceived individual’s dominance ranking in a social hierarchy, as rateJ by human judges observing the group’s social behavior. Waveform peak components to monkey and human faces showed similarities in their spatial distribution. However, larger amplitude Nl and N2 components were elicited in response to monkey compared to human faces, particularly over lateral temporo-parietal sites. A similar trend was observed for the P3 component, with maximal differences along midline electrode sites. Responses to familiar and unfamiliar monkey faces showed larger Nls to familiar monkey faces and larger P3s to unfamiliar monkey faces. Nl and P3 components elicited by human faces showed no

significant differences between conditions. N2 amplitudes were larger over posterior sites for top-ranked monkeys and larger over frontal sites for middle-and bottom-ranked monkeys. Top-ranked human faces elicited the largest N2 components, midtlle-ranked faces the next largest, and bottom-ranked faces the smallest. Nl, N2, and P3 latencies were similarly sensitive to the ranking of human but not monkey faces. These data suggest that non-human primates exhibit evoked potentials to conspecific and non-conspecific faces that are similar in morphology but different in function. Larger amplitude responses to monkey faces suggests increased processing for that category of stimuli. Additionally, monkey ERPs reflect familiarity with compecifics but not with human faces. Finally, the social status of the perceived individual, or at least the perceived threat posed by an individual, affects the latencies and magnitudes of ERP components produced by the viewer. These data are consistent with social attention hypotheses which propose that higher status (i.e. more dominant or socially meaningful) members of a gr0L.p reccivc more attention than lower status individuals. Key words:

Monkey; Social status; Hierarchy; Event related potential;

1. Introduction The ability to recognize faces quickly and efficiently is important for communication among humans becauxe it provides large amounts of information about the perceived individual in a complex social situation. Information can be gained regarding the identity, gender. emotional state, age, expression, and intent of the person [l&19]. Since a number of behavioral studies havl2 shown that non-human primates live in communities in the wild involving very intricate social structures [1,15,37], it would be expected that face perception and

* Glrresponding

author.

Fax: (1) (619) 534-l 128.

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Nl; N2; P3

recognition would also play an important role in their social interactions [ 12,341. Indeed, non-verbal mimic expressions and gestures are prominent communicative signals that regulate monkey social communication. In particular, one aspect of non-verbal communication that is critical to the interactions among non-human primates is recognition of the social status of the perceived individual [7,21]. It has been noted by several investigators that when viewing other conspecifics, monkeys elicit responses appropriate to the perceived individual’s social status [11,20]. This type of social attention is essential for dyadic interactions among group members, as well as for the coordination of group activities [391. Non-human primates will also respond to pictoral stimuli as if

to the real object [ 11,20,34]. Chimpanzees, for example, have been shown to recognize photographs of humans with whom they share a strong social relationship [lo]. Several studies have argued that high status members in non-human primate social groups are typically the center of attention [14,23]. However, a number of human and animal studies have failed to find an association between dominance status and social attention [39,40]. In general, these type of studies suffer from a lack of a clear operational definition of social attention, a lack of support for the notion that social attention refers to a single concept, and the lack of a rigorous method for evaluating the behavior. Hence, it would bc useful within this framework to examine the relationship between social status and a more clearly defined dimension of social attention, such as face recognition. Furthermore, a technique to record brain electrical activity, such as event-related potentials (ERPs), that would be sensitive to the temporal dynamics of these processes would be useful. Previous studies have shown that specific aspects of face processing can be characterized by ERPs in humans [3-5,241 and monkeys [31,32]. These studies indicate that ERP indices of face perception and recognition can reflect the analysis of familiar and unfamiliar conspecific faces [3 1,321. They also indicate that human and monkey ERPs to faces are typically largest near the superior temporal sulcus (STS) in temporal cortex [9,24,31]. This is consistent with single cell studies of face recognition in non-human primates which support the hypothesis that specific cell populations in the superior temporal polysensory area (STP) of STS and in the inferior temporal cortex (IT) respond singularly to the configurational aspect of faces [6,13,17,18,22,25]. Cells in these regions respond independently of species, head orientations, facial components, changes in size, contrast. color, or viewing distance [30,33]. Moreover, cells respond to real faces as well as to photographed ones [171. Recent evidence argues that cells which respond to identity may be segregated in the TEm subdivision of IT, apart from cells which respond to expression, which are found primarily in the TPO subdivision of STP [22]. This segregation of functionally distinct groups of cells, in combination with other cells that arc primarily sensitive to facial features, such as noses and eyes, give support to the idea of a face recognition network in temporal cortex [17]. Such a specialized detection and recognition system would be significant in a monkey’s ability to extract meaning from faces. The goal of this study is to examine whether face recognition in non-human primates, as an aspect of social attention, can be characterized electrophysiologically and whether this process is related to or affected by the social status of the perceived individual. To date, no ERP studies have addressed these issues. The

main questions to be answered are: (1) are there ERP differences in monkey responses to human versus monkey faces? (2) are there differences in their responses to familiar versus unfamiliar faces, i.e. whether conspecifics or not‘? and (3) does the social status of the perceived individual affect how they are perceived?

2. Materials

and methods

2 1. Subjects Subjects were six adult. male squirrel monkeys (Samiri Their

ages ranged from 7715 years and weighed

sc~urrw.~).

hetween

700~1000

g. All monkeys had taken part in previous ERP studies and had prior interaction

as a social unit. Only four of the monkeys had implanted

electrodes

to measure

the

electroencephalogram

(EEG).

maining two monkeys were used in the behavioral to determine

Monkeys

had been implanted

In

monkeys

(SO mg/kg

artificially

I/min).

respirated

were

Cm.)

was maintained

oxygen (1~1.5

with an array of electrodes

to this study (see Pineda

summary,

hydrochloride Anesthesia

re-

social rankings.

least one year prior details).

The

part of the study

anesthetized

and

atropine

with isoflurane

for at [31] for

using ketaminr

(0.05

mg/kg

tO.S-1.5%)

i.m.).

mixed with

while the animal was on a heating blanket (12-15

and

breaths/mink

Subjects were placed in a Kopf stereotaxic aseptic surgical procedures skull was resected,

and Nava

apparatus,

and using

the skin overlying the dorsal aspect of the

the underlying

muscles retracted,

and an array of

small stainless steel screws (00 gauge, 1.5 mm length) were threaded into burr holes in the skull. Wire

leads from these electrodes

attached

and electrodes,

to a multi-pin

connector,

tor were

fixed

cylinders

(5.7 cm long, 0.8 cm in diameter)

to the

skull with

dental

acrylic.

use in fixing the head during experimental

2.3. Experimental

were

leads and connecTwo

small

were attached

metal

for later

sessions.

paradigm

As shown in Fig. I. stimuli consisted of 140 color slides of real human

and

squirrel

monkey

ground was darkened of 35 unique, man

unfamiliar

faces (i.e.

memhers

who

human

multiple

presented

with

squirrel

and monkey

the

familiar

into 10 slides of the top-ranked slides of the middle-ranked ranked

hack-

of faces

monkeys

familiar

belonging

on a daily basis), 35

representations faces were

individual

individuals,

hu-

to lab famil-

of roommate

further

subdivided

in a social hierarchy,

IS

and 10 slides of the hottom-

individual.

Slides were presented puter controlled automatic

Kodak

pseudorandomly Ektagraphic

for 500 ms using a com-

Projection

shutter. They were hack-projected

distance of 64 cm onto a translucent Subjects viewed the images through acoustically

isolated

chamber

(1st)

occurred

between

Tachistoscope

with

at a slight angle from a

screen in front of the subject. a glass window

at a distance

tended a visual angle of approximately interval

The

monkey faces, and 35 non-unique,

iar. squirrel monkey faces (i.e. multiple faces). Human

upright.

faces, 3.5 non-unique,

presentations

interacted

unique. unfamiliar,

faces

so that only faces were visible. Slides consisted

from within

of 34 cm. Images

an sub-

9.5” X 9.5”. A 4-s interstimulus

slides. ERPs

session for each subject. Lights were turned and in the outer room during the experiment.

were

recorded

in one

off inside the chamber

J.A. Pineda et 01. / Cogniti~3e Brain Research

PARADIGM

2 (1994)

3

l-12

monkey

limbs away from

monkey

subjects were placed inside an acoustically

attenuating

chamber.

their

faced

monkey‘s head to relay signals to the EEG

the screen.

recorded

'70

A cable was attached

were analogous

tional Electrode ment lateral

(MONKEY)

(HUMAN)

/\

(T3,

T4,

(FAMILIAR)

/I\15 10

P3, P4) sites. Electrode> sites were

10

(MIDDLE)

(BOTTOM)

ITOP)

I,

Fig.

Schematic

(BOTTOM)

of the paradigm

with 70 human

of faces were further

and 35 familiar

(MIDDLE)

(TOP)

of the structure

slide\ were presented two categories

10

faces. Additionally,

familiar

hierarchy that was determined

placedata.

placed

referenced

in the bony orhit

blinks and other eye

to an electrode

implanted

1-2 mm below the inion. data were amplified

using 7PSB pre-amplifiers EEG

on-line

by a Grass model 7D

with handpass limits of 0.15 Hz

activity time-locked

to stimulus presentation

for 100 ms prior to and 900 ms following

wah

stimulus

disk for later analysis.

2.6. Data rrnalysls

in which 140 total faces. These

into 35 unfamiliar

faces were

subdivided

into lop, middle. and bottom ranked individuals according to a social dominance

ERP

onset at a sampling rate of 256 Hz. Data were stored on a computer

and 70 monkey subdivided

aitea

Interna-

(Fz, Cz, Pz, Oz) and four

All

and 35 Hz.

/I\15 10

and human

movements.

digitized

on the

Electrode

hy the IO-20

to hoth eyes were used to monitor

polygraph

(FAMILIAR)

of monkey

from four midline

Eight channels of EEG (UNFAMILIAR)

to the connector

dorsolateral approximately

sound

so that the monkey

System. This system for electrode

comparison

Signals were recorded

in the chair.

shielded,

polygraph.

to those described

Placement

allows direct

seated

The chair was positioned

TOTAL

70'

MILIAR)

Once

SLIDES

140

(UNF!

heads.

from individual

behavioral

prof les.

ERP

averages were obtained

key faces),

familiarity

(familiar

familiar

and

unfamiliar

middle,

and

bottom

Grand

averages

conditions.

An

based on species (human and

monkey

ranked

faces),

human

across subjects artifact

rejection

movements

occurred)

movements.

The

were

latency

human social

monkey

calculated

and monfaces and

ranking familiar

for

(top, faces).

all of these

was used to reject

EEG

i 75 PV (i.e. where blinks or eye

or when amplifier

following

and

and

program

trials in which the voltage exceeded 2.4. Social hierarchy

unfamiliar

blocking resulted from such

windows

(in ms) were

obtained

from visual inspection of the grand averages and utilized for measurRanking

the six monkey subjects on a social hierarchy

on observations month.

conducted

was based

during ten sessions over the course of a

All subjects were

placed

in a large cage consisting of two

ing the largest positive (P) or negative (N) peak within the interval: NI (60-200); tudes (PV)

N2 (200-400);

P3 (250-600).

Latencies

(ms) and ampli-

were scored for all peaks, while area (PV-ms)

was only

amo.lg the group were noted by an observer standing approximately

data were automatically scored, although for approximately 10% of the data records, manual scoring was required. The largest peak amplitude within each window was measured relative to the mean voltage in the IO0 ms prestimulus interval. Latencies, amplitudes, and areas were analyzed using repeated-mensure analyses of variance (ANOVA) with factors of species (2),

5 fe~:t in front

familiarity

contiguous,

large (5’ X 3’ X 3’) cages that contained

ropes, and a water

bottle.

actic,ns and identifiable

branches,

Subjects were easily recognized

markings.

Natural

toys,

by their

behaviors, including domi-

nantc gestures, signs of aggression or submission, displays of authority, ,Inti-social

behaviors,

vocalizations,

of the cage. Observations

monkey initiated 111separate made

were

sessions, the observer

as to the

monkeys obtained

made

as to which

manipulated

(2), ranking (3). and electrode

placement

(8).

the environment

of food in the playground.

level

of competition

for

Observations

the

food,

which

3. Results

the food, and the order in which it was obtained.

In a few instances, to clarify the relationship middle

of interaction

for P3. The

an action and who was the target of that action.

by placing small quantities wert

and patterns

obtained

of the hierarchy,

among monkeys in the

pairs of monkeys were placed

3. I. Monkey dominance

rankings

in a single

cage to more closely observe their interactions. Iamiliar

human

faces were categorized

based on the monkeys’ These reactions

included

‘fear’

reaction

cowering.

in terms of a hierarchy

to the perceived

avoidance

mov ng to the back of the cage, and baring when

of direct eye contact, of teeth.

the subjects found to be most threatening

top, the least threatening middle

rank.

Such

a structure

hierarchy,

The

person

(JP) was coded as

person. who elicited the least reaction,

coded as bottom (GS), while the remaining dominance

individual.

is not

analogous

but it was important

was

faces were coded in the to the

to maintain

monkey

a balanced

paradigm. 2.5. I:EG

recording

Monkeys chai: limited

were

protocol first acclimated

and to the experimental movement

and included

to a specially

setup.

The

designed

primate

chair was designed

a restrictive

collar

that

kept

for the

A schematic of the social hierarchy developed from behavioral observations is shown in Fig. 2. This dominance hierarchy was the result of observations and analysis by the second author (G.S.) with verification by the other authors. The results indicate that there were at least three levels of dominance in the hierarchy. The top level was occupied by Grandpa, the oldest (approximately 15 years), unimplanted, and clearly the most dominant squirrel monkey in the colony. He is the largest animal, shows the most aggressive behavior, is rarely challenged, and is typically the first to eat. The middle ranked animals consisted of Peter, Kive, Chomp and Ziggy. Differences in behavior among these four monkeys were subtle, inconsistent, and it was unclear

J.A. Pirleda et 01./ Cognitirv Bruin Re.warch 2 (19941 I-12

3.2. Human

HIERARCHY GRANDPA

/\ PETER

KIVE

ZIGGY

CHOMP

\/ UELI Fig. 2. Schematic of the social hierarchy observed among six laboratory monkeys as judged by three raters. The lack of a clear relationship among some of the middle ranked monkeys (e.g. between Peter and Kive) suggested a two-path rather than a linear relationship. Grandpa was clearly the most dominant, while Ueli was clearly the most submissive. These relationships were constant throughout the study.

as to what the exact relationship was among them. For this reason, the linear dominance hierarchy that is typically expected to exist has been drawn with two paths. The lowest level was occupied by Ueli, an implanted monkey, approximately 11 years old. He was typically the least aggressive, the last to obtain food, and the most submissive of all the animals. The social rankings determined from these observations remained stable throughout the duration of the study.

IX monkey fuces

Grand average ERPs to human and monkey faces are shown in Fig. 3. The waveforms include an Nl-P2N2-P3 complex that was most clearly visible at the vertex (Cz> site. Nl (mean latency of 103 ms to both human and monkey faces) was masked by a large positivity over frontal cortex, while exhibiting maximum amplitude over temporal sites. N2 (mean latencies: 1X2 ms for monkey faces; 194 ms for human faces) was largest over frontal cortex while P3 (mean latencies: 307 for monkey faces; 290 for human faces) achieved maximum amplitude over posterior midline sites. P3 latencies decreased from front to back by a total of 30 ms. The similarity in the spatial distribution of Nl amplitude responses to human and monkey faces is illustrated in the left column of Fig. 4. Table 1 shows the mean amplitudes and latencies of all the measured components. Increasingly larger Nl responses to human and monkey faces occurred from front to back along midline sites (electrode placement, F,,z, = 13.77, P < 0.001) with no between category differences observed. Monkey facts elicited larger amplitude Nl components at lateral sites (species x electrode placcment, F,,*, = 4.00, P < 0.01). Larger N2 components were also elicited primarily over lateral electrodes in response to monkey compared to human faces (species x electrode placement, F,,z, = 2.81, P < 0.05). Like Nl, the topography of N2 amplitude responses was similar for both categories of faces (see right column of Fig. 4). That is, N2 decreased in amplitude from front to back along midline sites (electrode placement, F,,?, = 8.22, P < 0.001) with no between category differences. No

Monkey

Fig. 3. Grand average ERPs from four adult squirrel monkeys to upright human and monkey faces. Waveforms are presented from three midline (Fz. Cz, Pz) and two lateral temporal (T3. T4) electrode sites. Note the similarities in waveforms and peak latencies and the enhanced response to monkey faces.

J.A. Pineda et al. / Cognitille Brain Research 2 (1994) I-12

N2

Nl 20 7

20 -

rJl

0 z

-20 - +

-

9 “a -40 -

_

I -60 -

-60 -

-80 -

-80 -

-100

-100

’ ’ ’ ’ ’ ’ ’ ’ Fz Cz Pz Oz T3 T4 P3 P4 Electrode Sites

0

Monkey 0 Human ’ ’ ’ ’ ’ ’ ’ ’ Fz Cz Pz Oz T3 T4 P3 P4 Electrode Sites

Fig. 4. Distribution of Nl (left column) and N2 (right column) amplitudes (pV) in response the ,?patial distribution of Nl and N2 amplitude responses to the two categories of faces.

to human

and monkey

faces. Note the similarities

in

The grand average ERPs to familiar and unfamiliar human and monkey faces are shown in Fig. 5. Table 2

shows the mean amplitudes and latencies for all components as a function of familiarity. Nl amplitudes were marginally different in response to familiar and unfamiliar monkey faces (familiarity, F,,, = 6.34, P = 0.086). Larger responses occurred to familiar (-38 pV> compared to unfamiliar (- 24 pV> faces. No statistical differences were observed in response to human faces, although the ERP grand average data showed an opposite trend, that is, larger Nl responses to unfamiliar human faces. N2 amplitudes and Nl latencies also did not show any statistically significant differences between familiar and unfamiliar conditions for either human or monkey faces. In contrast, N2 latencies were

Table 1 Me; II latencies

to human

statistically significant differences in Nl or N2 latentie! to human and monkey faces were observed. Likesignificant differences were obwisl:, no statistically tained for P3 amplitude or area, although amplitude responses to monkey faces were larger than those for human faces by 8 PV at Cz and 10 PV at Pz (see Fig. 3). Area responses also showed the largest difference (1800 PV-ms) at Pz. 3.3. Familiar us. unfamiliar faces

(ms) and amplitudes FZ

(PV) for Nl, N2, and P3 in response CZ

PZ

OZ

and monkey

faces T4

T3

P3

P4

Nl L ltency Human Monkey Amplitude Human Monkey N2 L itency Human Monkey Amplitude Human Monkey P3 L itency Human Monkey Amplitude Human Monkey

98 94

85 102

108 107

108 102

104 98

101 104

104 102

118 115

- 11.2 ~ 12.5

- 19.3 ~ 26.2

- 12.0 - 16.8

- 17.6 - 22.8

- 52.6 - 77.2

- 53.8 -6X.7

- 14.1 ~ 30.0

196 188

188 188

195 185

192 175

206 182

186 176

1x9 182

204 176

- 6.0 -21.9

- 4.6 - 10.9

- 1.2 - 5.8

1.4 - 2.2

- 14.2 - 34.1

- 13.9 - 26.7

- 15.3 -27.1

~ lY.5 - 39.9

284 304

284 290

279 280

265 265

300 320

300 322

308 356

301 323

0.0 12.0

10.0 12.4

13.9 21.7

21.6 31.6

23.6 28.5

9.4 11.8

10.1 11.4

10.8 12.3

12.4 13.5

at least 13-20 ms faster to unfamiliar faces at lateral electrode sites (human: familiarity x electrode place= 2.51, P < 0.05; and marginally significant ment, F,,, for monl&y: familiarity x electrode placement, F,,z, = 2.20, P < 0.08). Larger amplitude P3s were observed in response to unfamiliar (21.7 FV) compared to familiar ( 17.1 FV) monkey faces (familiarity, F,,, = 17.11, P < 0.05). No other statistically significant differences in P3 amplitude, latency, or area occurred.

while mean latencies and amplitudes for all components in these conditions are shown in Table 3. There was a main effect of ranking on Nl latencies to human faces (ranking, FL,<,= 6.90, P < 0.05). That is, bottom ranked human faces elicited faster latencies (88 ms) than either middle (99 ms) or top (99 ms) ranked faces. No statistically significant differences in ranking were observed for Nl amplitude or latency in response to monkey faces, nor was there an effect on Nl amplitude to human faces. N2 amplitudes showed a marginally significant main effect of ranking in responses to human faces, with top-ranked faces eliciting larger ( - 3 1.1 PV) responses than middle ( - 7.1 PV) or bottom (4.2 PV) ranked faces (ranking, (F,,, = 3.87, P = 0.08). As

3.4. Social rank&s Grand average ERPs to top, middle, and bottom ranked human and monkey faces are shown in Fig. 6, *rahlc ? Mean Iatencies (ms) and amplitudes FZ

(WV) for Nl, c/!

N2, and P3 in res~onsr PZ

to

02

familiar

and unfamiliar T3

human and monkev faces T4

P3

P4

Nl Latency fluman Familiar

97

YX

107

I IO

96

IO2

I02

I14

Unfamiliar

YX

X4

III

IIX

I06

IO3

I06

11x

Familiar

YO

IO I

101

100

I04

I OS

102

I 10

Unfamiliar

03

104

I03

IO3

IO.?

I Oh

Monkey OX

Oh

Amplitude Human Familiar Unfamiliar

6.9 ~ 0.3

~ X.6 ~ IS.9

-

15.2 _ 23.5

-x.7

-

IS.6 _ 21.x

-4Y.l

-4x.x

- Il.6

~ S7.0

~ 60.0

IO.6 _ 73.2

-

Monkey Familiar Unfamiliar

I I .o

~ IX.7

-21.x

-35.2

~ X2.7

-7x.4

-

Y.5

~ IO.9

- IS.5

- IS.‘)

~ 4Y.O

-61.7

-21.1

44.0

N? Latrncy Human Familiar

IYY

I75

IX4

I OX

21.1

204

211

IX8

Unfamiliar

194

IXX

lY2

17x

IXX

100

I74

I90

Familiar

lxx

I90

IX’)

I77

IX4

IYX

203

177

Unfamiliar

IX7

IX5

17s

17.3

177

172

I74

176

Monhq

Amplitude Human Familiar

~ I.9

I .h

~ 14.6

- 13.5

Familiar

- 26.3

- 13.3

Unfamiliar

- IO.3

- IO.1

Unfamiliar

2.3 6.0

- 12.8

~ 10.7

~ 12.0

~ 12.1

- 0.3

I.‘)

-21.4

- IX.2

~ 24.5

~ 29.2

13.6

- 6.5

~ 49.5

~ 32.0

~ 35.0

- 45.5

- 2.0

I.2

- 26.7

~ 2S.2

72.5

- 35.4

Monkey

-

I’.? Latency Human Familiar

271

2x2

264

27.5

301

324

307

322

Unfamiliar

275

28’)

31X

295

28X

303

310

312

Familiar

30x

297

2x1

so0

323

345

361

345

Unfamiliar

304

300

30s

2x0

326

323

364

322

Monkey

Amplitude

I luman Familiar Unfamiliar

13.7

17.7

245

22.h

6.X

10.x

22.6

2Y.O

14.2

17.2

14.3

16.4

7.6

X. I

7.7

I I.5

I I.3 16.0

23.7

3.73

23.2

32.3

2h.O

Y.h

I I.h

10.2

IO.‘)

35.0

19.X

15.x

17.x

13.5

Monkey Fnmillar Untamiliar

J.A. Pineda et al. /Cognitive

Brain

Research 2 (1994)

Monkey

I-12

Human

_ _. 5;s

(jfl/zam;,;ar

_

200

400

600

800

mscc

Fig. 5. Grand average ERPs from four monkey subjects in response to familiar and unfamiliar monkey (left column) and human (right column) face-. Waveforms were recorded from four midline (Fz, Cz, Pz, Oz) and four lateral (T3. T4, P3, P4) electrode sites but only three midline sites are ,,hown.

shown in Fig. 7, N2 amplitude responses along midline electrode sites decreased in amplitude for bottom and middle ranked monkey faces, but increased in amplitude for top ranked monkeys (ranking x electrode

placement F,, 42 = 2.36, P < 0.05). N2 latency did not show any significant differences to monkey rankings but did exhibit a linear relationship for human rankings, primarily over temporal sites. This relationship

Monkey

Human

TOP 5yv

_

... .. .. ... .. .... .. ... .

(f/f,&+

..~~~.._...

Bottom

,

200

400

600

800

msec

Fig. 6. Grand average ERPs from four monkey subjects to top, middle and bottom ranked Wa;,eforms from three midline (Fz, Cz, Pz) electrode sites are shown: ‘Note the sustained

monkey (left column) and human difference in response to human

(right column) faces.

faces,

x

J.A. Pitwdu

et ~1. / Cogniriw

Bruin

Rexwrch

2 (19941 I-12

between top, middle, and bottom ranked monkey and N2 latency, in which latency decreased from top to bottom rankings, is shown in Fig. 8. P3 amplitude and

area were not significantly different as a function of ranking for either human or monkey faces. Neither was P3 latency for monkey faces. However, for human faces

Table 3 Mean latencies hierarchy

to familiar

(ms) and amplitudes FL

(PV) for Ni, N2. and I’3 in response

cz

PZ

OZ

faces ranked

T3

as the top, middle.

T4

P3

and bottom

of B social

P4

Nl

Latency FIuman Top Middle Bottom Monkey Top Middle Bottom Amplitude Human Top Middle Bottom Monkey Top Middle Bottom N2 Latencv Human Top Middle Bottom Monkey Top Middle Bottom Amplitudr Human Top Middle Bottom Monkey Top Middle Bottom P3 Latrncy Human Top Middle Bottom Monkey Top Middle Bottom Amplitude Human Top Middle Bottom Monkey Top Middle Bottom

X2 97 hS

I02 IO6 92

I04 9x 91

I10 1OS 74

90 90 X3

IO0 ox IO4

100 92 I02

IO2 I04 YS

YY 94 x3

104 100 92

102 I08 YS

104 I02 ox

104 107 ox

IO2 100 YS

II8 IIS I IO

3.X 12.0 I2.S

~ 19.4 ~ IO.5 0.0

- 9.5 ~ 19.0 - 6.5

- 19.1 - II.6 - IO. I

~ 32.x - 19.1 -21.0

- 60.7 - SO.8 -41.9

~ 53.0 ~ 55.0 ~ 45.0

_ 22.3 _ 22.3 -5.7

- 0.4 - I.7 2.2

-33.7 - 20.7 - 20,s

- 44.1

~ 25.3 -32.1

-3x.4 - 16.1 ~ 18.5

~ 42.9 - 40.4 - 34.2

- 76.6 ~ XX.4 ~ 73.2

~ x4.4 - X.5.h - 64.0

- 73.5 - 47.3 -36.X

202 I80 189

200 177 192

20’) 182 208

206 I64 220

203 I96 I72

211 lY4 IX5

203 177 191

200 206 1x3

193 191 176

1x1 190 210

17x I 04 210

174 IX.5 200

I76 IX6 20x

I70 208 207

I73 203 I Xh

I70 212 1x0

~ 24.6 - 5.2 14.9

_ 23.6 3.X 6.7

- 20. I 5. 2 4.4

~ 44.3 - 13.x 0.8

_ 2x.7 - KY ~ 0.7

~ 30.7 ~ 13.7 ~ 3.6

- 4x. 1 - IX.9 H.h

-X.4 -2X.3 ~ 20.6

_ 25.3 - 10.7 _ 21.5

~ 27.7 ~ 1.5 - 7.9

-33.4 -57.6 ~ 52.6

-34.X - 37.6 - 24.0

-31.‘) ~ 44.6 ~ 26.0

~ 69.9 -46.1 ~ 35.4

288 276 297

288 264 2X3

319 31x 270

300 32x 268

2YS 314 334

2X5 304 327

20s 29s 34s

32s 33x 3 I0

2X7 320 327

302 32s 306

314 321 30x

300 283 30x

324 324 31.5

307 327 322

303 337 309

34x 324 320

x5 6X 79

~ 2’). I ~ 4.9 IO.8

7.x 20.X 21.3

S.h 23.1 32.4

21 .o 32.2 41.4

17.5 34.5 35.6

5.0 24.7 24.7

5.5 20. I 29.7

3.6 1Y.0 33.3

6.0 19.6 31.h

31.0 17.0 Y.9

51.4 25.1 19.1

41.5 44.0 24.2

24.0 40.5 21.0

25.2 7.1 0.2

30.6 10.0 16.6

28.1 4.7 IX.5

30. I 6.6 13.4

J.A. Pirwdu et ul. / Cognitiw

N2 O,’

0

,’ ,’

_. > 2 82.

-10 .J

.I

.I ,,

d’ #’

‘\ ‘\ ‘\ ’ ‘\ I’ #” .\ #’

/’ -20

-

‘La I

.L_.__.

-30 .’

/

-40 ’

.’

.’

0 Top

d’

0 Middle

I Fz

I

1

I

Cz

Pz

Oz

W Bottom

Electrode Sites Fig. _. Distribution of N2 amplitudes along midline sites (Fz, Cz, Pz. Oz) in response to top, middle, and bottom ranked monkey faces. Note the difference in anterior-to-posterior gradients between responses to top ranked faces (which increase in amplitude) and responses to middle and bottom ranked faces (which decrease in amplitude).

there was a significant P3 latency effect (ranking X electrode placement, (F,,,,, = 2.00, P < 0.05). Like N2 latency, there was a linear relationship between ranking ;md P3 latencies at T3 and T4, as shown in Fig. 8, although P3 latency generally increased with decreased social rank.

4. Discussion 4.1. Social status and face recognition The sensitivity of squirrel monkey Nl, N2 and P3 latencies and amplitudes to monkey and human faces ranked at the top compared to those ranked in the middle or at the bottom of a social hierarchy is consistent with other studies of face recognition in non-human primates [lO,ll]. This, however, is the first known

Bruin Resrurch

2 (1994)

I-12

9

report of a relationship between ERP components elicited by face recognition and the social status of the perceived individual. The electrophysiological differences observed cannot be accounted for by physical features of the stimuli since pictures were equated for retinal size and general composition. Thus, the present data are consistent with social attention hypotheses which suggest that status in a social group is a determining factor in the amount and quality of attention received [14]. Behavioral studies typically characterize this type of social attention by the amount of visual monitoring that occurs [39]. This enhanced monitoring and ability to recognize status in a hierarchically organized group has been shown to confer advantages to the observer [38]. Monkey ERP component peaks are sensitive to the sensory, perceptual, and cognitive dimensions of sensory processing 131,321. The fact that latencies and amplitudes of long-latency components differentiate social rankings in human and monkey groups offers another way to define aspects of social attention. It can also serve as a tool for studying the neural substrates of such high-level processes. One troubling question about studying animals in captivity is the extent to which captivity itself might influence the social organization and patterns of behavior observed in field studies. Recent investigations indicate that social organization in non-human primates is changed little despite changes in the amount of living area, concentration of resources, and visual openness [29,351. If anything, confinement appears to intensify the social relationships. Studies of social dominance in captive populations, especially squirrel monkeys, also indicate that such relationships are typically linear and quite stable [16]. Dominance hierarchies have an important adaptive value. They allow individuals to predict the outcome of an interaction when there is both competition for scarce resources [261 or cooperation for mutual benefit [15]. However, recent questions have been raised as to whether monkeys actually ‘know’ their social status or

N2

P3

400

300 3

E

L9 TOP

0” 200 5 2 100

0I--

T3 T4 Electrode Sites

0

0

Middle

n

Bottom

T4

T3 Electrode Sites

Fig. 8. Histogram of N2 and P3 latencies from lateral temporal sites (T3, T4) in response N2 latencies decrease from top to bottom, P3 latencies increase.

to top, middle,

and bottom

ranked

human

faces. While

those of their partners [7,8,15]. It is certainly the case that many non-human primates show hierarchically organized relationships in terms of signs of aggression or submission and displays of authority, and these relationships tend to be stable [I(,]. Therefore, some form of hierarchical discrimination might be expected. The differences in ERPs observed in the present study, particularly long-latency components such as the N2. to a top versus lower ranked monkeys supports the hypothesis that differences, whether at an individual level or at a categorical level (i.e. very dominant, dominant, subordinate, very subordinate) are perceived, although not whether an animal is cognizant of it. Investigators have argued that the perception of differences in social rank means that some type of mental representation must be involved, allowing monkeys to make comparisons and draw inferences about social relationships. Furthermore. this type of knowledge in humans is typically declarative rather than procedural. However, the lack of distinct vocalizations for these relationships in most non-human primates argues that monkeys may not be aware of such knowledge [ 15.37]. Squirrel monkeys’ visual perceptual skills are fundamentally similar to those of Old World monkeys, apes and humans [27]. However, evidence from field research suggests that they live in a troop structure where the dispersion of adult males seems to bc associated with a predominantly cohesive female nucleus [2]. To that extent. their social organization differs from that of Old World. terrestrial species. Nonetheless, the prcscnt elcctrophysiological data are consistent with the behavioral findings that many monkeys respond to perceived conspccifics based on their social status [ 11,20.34]. The electrophysiological effects are evident at least as early as 100 ms following stimulus onset, at least in the perception of human faces. and are widely distributed throughout the cortical mantle. The widespread topography of these effects, as well as the apparent enhancement of both positive and ncgativc ERP components, suggests a generalized enhancement in the processing of faces throughout a variety of cortical areas. This is consistent with the idea of an attcntional bias in a distributed network involved in the perception and recognition of meaningful faces. The ERP responses to human faces as a function of their ranking is surprising because the premise for this hierarchy was not considered analogous to that used to rank monkey faces. Because human rankings were based primarily on the threatening nature of the pictured individuals. the systematic change from top to bottom. would be consistent with this categorization. It thus may be that threat. or the possibility of threatcnis one of several factors involved in ing behavior, establishing monkey social dominance. The sustained difference in response to human faces ranked as top, middle. and bottom of the hierarchy, which occurs

immediately after stimulus presentation, argues for a generalized, non-specific arousal effect. What is surprising is that these differences begin so early. A type of priming effect would explain such an early onset. However. the random nature of stimulus presentation would not prime subjects to respond one way or the other to the faces. It is possible, therefore, that categorization of the stimuli (i.e. very threatening, somewhat threatening, not threatening) occurs early on in the stream of processing, perhaps at some subcortical level. It is fair to say that monkey Nl, N2, and P.3 components were all sensitive to the rankings of human t’accs, whereas only N2 was sensitive to the rankings of monkey faces. The additional effects to the human faces may bc related to the degree of threat perceived. This is an issue that needs further exploration.

The present results indicate that monkeys elicit larger Nl and N2 responses, and tend to elicit larger P3 components, to conspecific compared to non-conspecific faces. Both human and monkey faces elicit waveforms with similar morphologics and peak latenties. The main diffcrencc is the cnhanccd response to monkey faces. This additional gain or modulation is similar to the cnhanccd processing of the top ranked monkey compared to the bottom ranked one and may retlcct enhanced attentional processing to conspecifics. The similarities in spatial distribution and in peak latencics but differcnccs in the magnitude of the response would suggest that the same neural substrates arc being engaged in response to the two categories of faces. Such an interpretation is consistent with the study by Overman and Doty [28] in which monkeys differcntiatcd monkey and human faces from other classes of visual stimuli, suggesting a unique processing mechanism for the stimulus category. Results from single cell studies also show that STS cells respond to faces as a general category rather than to specific individuals (i.e. the ‘grandmother’ cell) [ 171. A number of explanations for the cnhancemcnt or bias can be postulated. One possibility is that innate mechanisms are hardwired to give special processing to monkey conspecific facts [XI]. Altcrnativcly, the social context and lifetime cxpericnce monkeys have in processing monkey and human faces would. in itself, be enough to give additional significance or meaning to those facts. One way to test whether prior cxpcriencc is sufficient to produce the type of generalized enhanccments observed in this study is to cxaminc responses to familiar versus unfamiliar facts.

The present results suggest that familiar and unfamiliar faces arc indeed processed differently within a

J.A. Pineda et ul. / Cognitiw

single category (i.e. monkey faces) as well as between categories (i.e. human vs. monkey faces). Monkey ERPs appear sensitive to the familiarity dimension but only for conspecific faces. Within this category, the differenccs in processing appear to be component specific. That is, familiar monkey faces produce larger Nls but smaller P3s relative to unfamiliar monkey faces. These effects could result from an additional, overlapping negative wave elicited by familiar stimuli. Thus, familiarity per se would not explain the generalized enhanced negative and positive peaks in response to monkey faces. The lack of statistical differences in response to familiar and unfamiliar human faces suggesls that monkey ERPs are unable to distinguish stimuli along this dimension. This implies that there exist distinct face processing mechanisms, or at least distinct processing strategies, for human and monkey facts. Why these differences in processing occur remains to be examined.

Bruin Rewurch

2 (I 994) I-12

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Recognition of faces is an important component of non-verbal human and monkey social communication. Because of the evolutionary link with non-human primates, it is reasonable to assume that the mechanisms by which social status is discriminated may still exist in humans. Such systems may have either retained their function or been adapted for more ethologically relevant human behavior, such as allocating attention, via fact recognition, to socially meaningful faces. Human relationships are typically not cast within the context of rigid social hierarchies of the type seen in non-human primate social groups. Some children studies report thar the most aggressive individuals in a group do not necessarily acquire the dominant status in the group. Other factors such as intelligence, skill in interpersonal relations, self confidence, and problem-solving abilities play just as important a role [41]. Nevertheless, some similarities remain. One issue to be explored by a human study is whether, and to what extent, humans are biased to process human faces. Furthermore, ERP stutlies in young children could determine whether sucv a bias is hardwired or simply a function of learning and of tuning a face processing neural network. The phenomenon in which individuals of a racial group, other than one’s own, are difficult to discriminate suggests that learning is critical in human face recognition.

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