Arousal, Activation, and Effort in the Control of Attention

35 Pages·2010·1.19 MB·English

Psydowf.icoJReview
1975 Yo. 82, No.2, 116-149
Arousal, Activation, and Effort in the Control of Attention
Karl H. Pribram
Stanford University
AND
Diane McGuinness
University College, London, and the Hatfield Polytechnic,
Hatfield, England
PIYC"/lkolR~
1975, Vol. 8l, No. l, IHI-149
Arousal, Activation, and Effort in the Control of Attention
Karl H. Pribram Diane McGuinness
Stanford University University College, London, and the Hatfield
Polytechnic, Hatfield, England
This review attempts to organize a range of neuropsychological and psycho
physiological data On attention. Three separate, but interacting, neural sys
tems are distinguished: One controls arousal, which is defined in terms of
phasic physiological responses to input. The arousal control circuits center
on the amygdala. A second system controls activation, which is defined in
terms of tonic physiological readiness to respond. The readiness circuits
center on the basal ganglia of the forebrain. A third system is discerned
which coordinates arousal and activation. This coordinating activity is
defined as demanding effort. Its cin;uitry centers on the hippocampus.
When arousal, activation, and effort are involved in problem solving, at least
two further distinctions can be made. During categorizing, arousal precedes
activation; during reasoning, activation precedes arousal. Finally, the review
addresses the Question of whether effort in problem solving is to be attributed
solely to peripheral muscular factors or whether, in fact, direct monitoring
of changes in brain organization (changes in set, attitude, etc.) can be
productive of measurable indicators of effort.
In the mid 1960s,R. J. Douglasand K. H. sensory events (orienting, vigilance, and
Pribram presented a series of experiments habituation) and (b) the invariant (cate
detailing the effects of hippocampal lesions gorizing), or the variable but computable
on problem-solving behavior. The results of (reasoning), pairing of the outcome of re
these experiments were accounted for by re sponse (reinforcement) to sensory events.
course to the concept of experiencing a An assessmentofthe data derived from these
change in awareness which was interpreted paradigms (in approximately 200 experi
as indicating the involvement of "attention." ments) has led us to identify three basic at
A continuing interest in problems of atten tentional control processes: One regulates
tion has been reflected not only in the work arousal resulting from input; a second con
reported from our laboratory (a dozen and a trols the preparatory activation of response
half papers) but also in that of many others mechanisms; and a third operates to co
(see reviews by Mostofsky, 1970; Horn and ordinate arousal and activation, an operation
Hinde, 1970; and Kahneman, 1973). Re that demands effort. The first two sections
search has largely been directed to two gen of this review will delineate these attentional
eral paradigms defined by the following op control systems; the last section will deal pri
erations: (a) recording the occurrence of marily with higher order corticalattentional
physiological or behavioral responses against controls that operate during categorizing and
a background of monotonous repetition of reasoning.
We wish to express our gratitude to Muriel REFLEX ATTENTION, REPRESENTATION, AND
Bagshaw for additional data analysis and for al THE CONTROL OF AROUSAL
lowing us to present her unpublished work in this
Arousal is said to occur when an input
manuscript, and to Linda Heider and Barbara
change produces a measurable incrementing
Honegger for their patient help. The research
involved was supported by National Institute of of a physiological (e.g., single unit record
Mental Health Grant MH-12970-08 and National ing of neural potentials; galvanic skin re
Institute of Mental Health Career Award MH sponse) or behavioral (e.g., response ampli
15214-13 to the first author.
tude of a spinal reflex; frequency of a loco
Requests for reprints should be sent to Karl H.
Pribram, Departmentof Psychology, Stanford Uni motor response) indicator over a baseline.
versity, Stanford, California 94305. The types of input change that produce
116
THE CONTROL OF ATTENTION 117
arousal have been studied extensively and ability of neural tissue as a consequence of
have been labeled by Berlyne (1969) as col experience seized on the habituation of an
lative variables. These include sudden initial neural or behavioral arousal reaction
changes in intensity to which the organism as an extremely simple test paradigm that
is unaccustomed, changes in the timing of suited this purpose. Although these efforts
inputs, and changes in the ground in which and results have been reviewed by Horn and
a stimulus figure appears, in particular when Hinde (1970), we will highlight certain is
input is scarce, surprising, complex, and sues that are relevant to this presenetation.
novel. Such collative characteristics also An approach initiated by Spencer and
define the concept "information" as it is used Thompson (see Groves and Thompson,
in the study of communication systems (see 1970) involved recording from the spinal
e.g., Brillouin, 1962); thus it is possible to cord and illustrated that neither sensory af
treat organisms subject to arousal as "in ferents nor motor efferents accounted for
formation processing systems," where input habituation of spinal reflex behavior. Fur
is matched against some residual in the or ther, Thompson discerned two primary sys
ganism of his past experience, or some com tems, two classes of neurons; those that re
petence (Miller, Galanter, &Pribram, 1960; sponded more slowly and incremented for
Pribram, 1971). Without such matching, relatively long periods before decrementing,
there could be no novelty or information nor and those that rapidly decremented their ac
even a measure of change in intensity. tivity with repetition of the stimulus. The
This knowledge has led to behavioral re incrementing "monitoring," "sameness," or
search which has been addressed to such is "arousal" neurons lie more ventrally and
sues as adaptation level (Helson, 1964), medially in the region of the origin of the
expectancy (Bruner, 1957) and the develop visceroautonomic outflow, while the decre
ment of "neuronal models" (Sokolov 1960, menting neurons lie, for the most part, in the
1963), while neuroscientists were able to dorsal horn of the spinal cord. Convergence
demonstrate the occurrence of a permanent of these two systems of neurons was as
or semipermanent modifiability of neural tis sumed to account for the activity of a third
sue (see Pribram and Broadbent, 1970; population of ("novelty") neurons whose
Horn and Hinde, 1970). response characteristics were identical to
those demonstrated by the reflex: arousal
Neural Modifiability
reaction, habituation, and dishabituation.
Sharpless and Jasper's (1956) and Soko Thompson's parallel processing model of
lov's (1963) classical studies paved the way arousal, habituation and dishabituation,
for an analysis of the requisites for produc shared by many other investigators (e.g.,
ing behavioral and physiological arousal re Horn, 1970; Segundo &Bell, 1970; Spencer
spomes. Especially significant was the im & April, 1970) is simpler than Sokolov's as
plication of information processing systems it depends only on spatial summation of
by Sokolov's findings (1963) that any arousal and decrementing. No "neuronal
change in a repetitively presented stimulus model" of the input is developed, only a
configuratioil would elicit responses even decrementing to repetition and an "arousal"
when that change was a shortening of the proportional to the strength of the input.
sensory input or the lowering of its intensity. The model does not account for Sokolov's
Sokolov concluded that the organism's sensi findings that in the intact organism dis
tivity was not just a measure of its threshold habituation occurs when stimulus duration is
but rather that sensitivity was a function of shortenedor stimulus intensity is diminished.
a match between input and some competence, These phenomena imply a hierarchical pro
a neuronal "model," or a patterned memory cess involvingstorageand subsequent match
trace developed in the br~in as a representa ingof input to store. Horn (Horn &Hinde.
tion of the experienced stimulus configura 1970) has developed a scheme whereby such
tion. Any mismatch produces orienting. a hierarchical process can be realized without
Many investigators concerned with modifi- any unnecessary assumptions that go beyond
118 KARL H. PRIBRAM AND DIANE MCGUINNESS
the data obtained by practically everyone; pIe auditory, visual, or cutaneous stimuli in
namely that the decrementing observed is the absence of hypothalamic stimulation.
due to self-generated synaptic depressionand Since these physiological changes are the
not to the development of inhibition (inhibi same as those observed in all orienting re
tory postsynaptic potentials characterized in sponses, the defense reaction could therefore
intracellular recordings by hyperpolariza be considered in part as due to an increase
tion). of arousal. .
This does not mean, of course, that inhibi
Sensory'SJ1stems and the Neuronal Model
tion fails to occur in many systems. The
sensory and motor pathways are replete with There is ample evidence that a host of
circuits that lead to both lateral (i.e., neigh other brain mechanisms are involved in the
borhood) and self-inhibition. As we shall orienting reaction. Electrical brain record
see shortly, habituation becomes organized ing, both with macro- and with, microelec
into patterns in these pathways whether by trodes, shows that initial desynchronization
the mechanisms proposed by Horn or by the and increase in neuronal discharge occurs in
action of inhibitory circuits, or both. a large number of neural systems. One of
the characteristics of familiarization con
Core Brain Arousal System
sequent on repetition of a stimulus is the
The rostral extension into the mesen progressive restriction of these sites (John,
cephalic brain stem of a column of medially 1967;John & Killam, 1960). Paradoxically,
placed cells accountsfor the well documented however, this restriction involves primarily
arousal effects ofstimulationsofthe reticular the sites where arousal neurons are located
formation (see Lindsley, 1961, and Magoun, and does not encompass either sensory path
1958 for review). Less well known is the ways or the primary sensory projection sys
fact that such effects are obtained even more tems where responses continue to be re
rostrally in the diencephalon in a continua corded in the habituated organism. These,
tion of this neuron system into the hypo therefore, became prime candidates for the
thalamus. locus of comparison of the input stimulus
The contribution of hypothalamic viscero configuration with the neuronal model regis
autonomic mechanisms to the reflexive as tered earlier through habituation.
pects of the orienting reaction has been To determine where the detailed compari
noted by Feldman and Waller (1962). The sons necessary to the Sokolovian model of
episodes of fighting and fleeing that are pro habituation and orienting might occur,
duced by electrical or chemical stimulation Grandstaff and Pribram (1972) studied the
to the so-called "defense" region of the hy possibility that Thompson's results pertained
pothalamus can be related to the orienting only to spinal cord and perhaps lower brain
reaction. Abrahams and Hilton 0958) and stem mechanisms but that at more rostral
Abrahams, Hilton, and Zbrozyna (1964) stations of the sensory projection systems,
found that. in attempting to produce a de patterns of change rather than simple dec
fense response by stimulation of the hypo rementing were produced during habitua
thalamus, at first, a much lower degree of tion. Surprisingly, this study showed the
arousal occurred, indicatedby pupildilatation Thompson model to hold at the collicular and
and postural alerting. Only when the level of thalamic levels: electrical responses recorded
stimulation was increased and maintained for from the lateral geniculate nucleus as well as
a few seconds did hissing, snarling, running, those from the retina and superior colliculus
and piloerection occur. In the later study, (also obtained with microelectrodes by Horn
alerting behaviors were measured in greater and Hill, 1966; and by Bures and Buresova.
detail, and during mild stimulation the 1970) in intact monkeys subjected to repeti
authors observed changes in pupil dilation, tive visualstimulationuniformly decremented
head movement, pricking the ears, respira to repetitive monotonous stimulation, and
tion, and blood flow. These same changes enhanced responses occurred only when a
were also recorded during responses to sim- change in stimulation was initiated. Soko-
THE CONTROL OF ATTENTION 119
lov's model was saved, however, by the re ing mechanism that relies on an initial simul
sults obtained from recordings of the activ taneous parallel processing stage, a problem
ity of visual cortex. Here, habituation which will be considered in the section on
produced no uniform decrementing-some categorizing. Here we first outline the
records invariably and reliably showed an in neural systems involved in the arousal and
crementing of activity, while others decre activation that leads to desynchronization of
mented (over each of many days of record the patternedneuronal model.
ing) and still others showed no reliable
Amygdala Circuits
changes. A patterned habituation response
occurred, and dishabituation to a change in There is evidence for the involvement of
stimulation disrupted this pattern. the amygdala and related frontal cortical
Patterned changes in cortical rhythmicity structures in the attentional control of the
also occur. Thus patterning of electrical core brain arousal systems. This evidence
brain activity is not limited to abrupt poten delineates two reciprocally acting circuits,
tials evoked by the stimulus. Earlier studies one facilitatory andthe other inhibitory, both
have been reviewed byJ.Mackworth (1969). converging on hypothalamic structures re
More recently it was shown that during lated to arousal. Such reciprocal innervation
habituation, changes occur in both latency allows sensitive modulation (tuning) of the
(increase) and duration (decrease) of de arousal mechanism.
synchronization when baseline activity is in In pursuing the question of which brain
the 10 Hz alpha frequency range (Bagshaw systems are involved in orienting and habitu
& Benzies, 1968; Grandstaff & Pribram, ation, we first replicated and showed some
1972). More complex frequency analysis of of the limits over which the Sokolov results
the ongoing cortical activity of limited areas held (Koepke & Pribram, 1966, 1967).
of the visual cortex (Grandstaff &Pribram, Whenadapting the techniques to the monkey
1972) has shown that a decrease in power
with habituation in 8-10, 37-50, and 72-80
Hz frequency ranges occurs when the ampli
tude of the evoked potential decreases. By 0---0 N
contrast, in those electrode placements where so Jrt••••••_ H
0·.··...········0IT
the amplitude of the evoked response in g······..·······OAH
creases, an increase in power in the alpha
and other critical ranges is obtained. These
patterns ofchangedo notoccurat subcortical 60
loci (optic nerve and lateral geniculate nu
AVG
c1eus) but are limited to recordings made PERCENT
from the visual cortex, supporting the con GSR
clusion that patterning of neuroelectric ac 40
tivity, an indication of the construction of a
"neuronal model," is primarily the function
of a cortital information processing com
20
petency.
The occurrence of a patterned response
at the cortex suggests that each of the cor
tical sitescan beconsidered separate informa
tion processing channels, which is consonant Z 3 4
10TRIAL BLOCKS
with the anatomy of these systems. Neisser
(1967), Kahneman (1973), and Lindsay FIGURE1. Curvesforoverallpercentageofgalvanic
(1970) have thoroughly reviewed the be skin response (GSR) tothe first 50presentationsof
anirregularlypresented2-sectone. (Abbreviations:
havioral evidence for considering the sensory
N=unoperated group; H =hippocampectornized
channels to be primarily parallel processing group; IT=control group; AM=amygdalectom
systems, or at least some form of multiplex- ized group.)
120 KARL H. PRIBRAM AND DIANE MCGUINNESS
80,...--'!:P----...l'l.-----r---, parallel behavioral orienting. In many in
stances the opposite was observed.
Resections of dorsolateral frontal cortex
always abolish the visceroautonomic com
ponents of orienting (Kimble, Bagshaw, &
60 Pribram, 1965; Luria & Homskaya, 1970;
w Luria, Pribram, & Homskaya, 1964), while
oCzi) amygdala, resections produce a bimodal dis
ll; tribution. Electrodermal responses during
w
IX: orienting (Figures 1 and 2; Bagshaw &
g; 6 HIPPOCAMPECTOMY
40 oCONTROL Benzies, 1968; Bagshaw, Kimble, & Pri
Cl
1/l. • AMYGDALECTOMY bram, 1965) are reduced in amplitude and
z
« amount for most subjects. However, certain
w
:E subjects show an increas~number and am
plitude of response (see Figure 3 and Table
20
i). Tonic heart ,rate is paradoxically ele
vated (see below), but all phasic heart rate
responses areabolished (Bagshaw& Benzies,
1968; Pribram, Reitz, McNeil, & Spevack,
OL-_...L... L..- ....l.._---J 1974).
1-7 8-14 15-21 Thus, reciprocal systems appear to be in
TRIALSOF2-SECPURE TONE volved-one apparently relates to the dorso
lateral frontal cortex since resections of this
FIGURE 2. Curves for a more detailed analysis
of the first 21 trials (split into 7-trial blocks) or structure im'ariably eliminate visceral-auto
percentage of galvanic skin response (GSR) to a nomic orienting responses. The other, op-
2-sec tone for the amygdalectomized, hippocampec
tomized, and unoperated monkeys. (See also
Table 1.) ~\
........ 0 AMYGDALECTOMY
",'" \ (Responders)
...... \ • AMYGDALECTOMY_
we found, contrary to expectation, that le 0'"" "(Non-responders,
sions of the mediobasal, frontolimbic fore \6 HIPPOCAMPECTOM
\
brain, and not of the convexity of the cere o INFEROTEMPORAL \
CORTEXABLATlON \
bral mantle, had a dramatic effect on mea o CONTROL \\ J
sures of orienting (Bagshaw, Kimble, & \
\
Pribram, 1965; Kimble, Bagshaw, & Pri
bram, 1965). \ I
Amygdalectomy results in a failure of ~J
behavioral habituation, producing an ever
recurring locomotor orienting reaction (Bag .... 0:J
~ ~I
shaw & Benzies, 1968; Schwartzbaum, Wil
son, & Morrissette, 1961). Such hyper
reactivity is also produced by lesions of the ........
........
orbital surface of the frontal lobe (Mettler .......
& McLardy, 1948; Ruch & Shenkin, 1943; ol.-_~ ~"'. _
Wall &Davis, 1951) which has been shown 1-7 8-14 15-21
to be a part of a larger orbitofrontal-insular TRIALOF2SECPURETONE
temporal-polar-amygdala system (Kaada, FIGCRE 3. Group mean amplitude for galvanic
Pribram, &Epstein, 1949). When an analy skin response (GSR) to tone on the first 21 trials
sis of the visceroautonomic components of showing the bimodal distribution of the amygdal
ectomized monkeys when compared with normal
the orienting response was carried out on
(control) and with two other brain-Iesioned groups
frontal and amygdalectomized'monkeys, it of monkeys: inferotemporal cortex resection and
was expected that these components would hippocampectomy.
~-~--------------.,....---
THE CONTROL OF ATTENTION 121
TABLE 1
AMOUNT AND AMPLITUDE OF GALVANICSKIN RESPONSES OVER TRIAL BLOCKSFORSUBJECTS
Response Amplitude
(%) (kD)
Group
Trials Trials Trials Trials Trials Trials
1-7 8-14 15-21 1-7 8-14 15-21
0:>
Xorrnal (14) 63 54 43 3.0 2.9 3.2
Hippocarnpectomy (7) 710 700 62 5.90 5.80 3.5
Arnygdalectorny (6)
Hyperresponsive (2) 90· 50 40 11.40 4.30 1.9
Hyporesponsive (4) 150 000 00· 2.0 I - -
No/e. "umberofsubjectsineachgroupappearinparenthesesfollowingthegroup.
•p <.05.
posite in function, is most likely related to input from locations near the visceroauto
the orbitofrontal cortex which has been nomic regulating mechanisms. This is borne
shown to be the rostral pole of an extensive out both by the results of electrical stimula
inhibitory pathway (Kaada, Pribram, &Ep tions of the hypothalamus (noted above),
stein, 1949; Pribram, 1961; Sauerland & the amygdala (Gastaut, 1953, 1954), andre
Clemente, 1973; Skinner & Lindsley, 1973; lated cortical areas (Wi1cott, in press).
Wall & Davis, 1951). These data relate Thus, not only can the visceroautonomic
to the early descriptions of the behavior of components of orienting be sharply distin
amygdalectomized animals (Pribram &Bag guished from the somatomotor components,
shaw, 1953) which focused on the fact that but their role in the orienting mechanism ap
while the majority were tame, unresponsive pears to be primary.
to threat, and nonaggressive, the opposite The fact that the two amygdala systems
finding was also occasionally observed (e.g., are reciprocal, one facilitating, the other
Rosvold, Mirsky, & Pribram, 1954), and inhibiting arousal, suggests a controlling,
more recent behavioral studies by Ursin and modulating mechanism and is in accord with
Kaada (1960) using restricted lesions and evidence on other control functions of the
electrical stimulations have confirmed the amygdala and related structures. Injections
stiggestion that at least two more or less of carbachol into the appropriate hypo
reciprocal systems can be identified in the thalamic site will initiate drinking; such in
amygdala. jections into the amygdala have no effect
unless the animal is already drinking, in
Attentiol1al Control of the Arousal System
which case the amount of drinking becomes
The presence of reciprocal systems sug proportional to the amount of carbachol in
gests the existence of a locus upon which jected in an exquisitely accurate relationship
they converge, a locus which, from anatom (Russell, Singer,Flanagan, Stone, & Rus
ical considerations (Pribram & Kruger, sell, 1968). The fr011toamgydala influence
1954), is most likely to be found in the can be conceived as a finely tuned determi
hypothalamic regions of the brain stem. nant controlling visceroautonomic arousal
This suggestion is supported by microelec initiated by the hypothalamic mechanism
trode evidence at the spinal cord level during orienting. It is as if in the absence
(Groves & Thompson, 1970) which indi of the frontoamygdala systems, the animal
cates that the origin of the desynchronizing would fail to control his drinking behavior:
mechanisnl'leading to orienting may be lo Once)5tarted he would drink under circum
calized to the medial parts of the spinal cord stances in which others would stop. This is
where the visceroautonomic outflow orig exactly what happens-and more. Both eat
inates. The neurons that respond during ing' and drinking are controlled in this
orienting are likely to have derived their fashion-not only their cessation but also
121 KARL H. PRIBRA~I .\XD DI.\XE :\IcGlT,XE:-S
100...-----------------, re~pon~t'sw movt'mellts or !() "hock. \\hen
.. thre"hold for shock "'as measured. iront:!1
lobectomized ~Grueninger .\: Grncninger.
1973) and nonresponsive am)'gcialenomized
/
............................~ subjects. ,,"ere found to have. if anything-.
;.." ........•....~ greater sensitivity (see Figure 4'). Specifi
.0'
o . cally. these mc'nkeys frequently t'roduced a
~
maximal number aed amplitude of re:-ponse:::
~40 /::....-------- •""- to intensities that produced very little or no
:i: :0 '~
reaction in normal subjects.
~
::20 : This leaves 1:0 doubt that the peripheral
response mechanism remains intact. ~either
ol-- a change in sensory sensitivity.. nor an al
:--~--:--..J
o J·4 4·a a·, '·4 4·.1 0 tered peripheral response mechanism can ac
d. SHO<l
count for the effects of frontal and 3m)'gdala
......AM lesions on the orienting reaction. The crit
-N
ical influence exerted by these forebrain
6Or----------------, structures appears to relate to arousal in
-- duced registration of input effecting changes
• ,.........•.. in the organization of central mechanisms.
~40 ........................... Certain changes relate to the finding that
.•.. despite reactivity to shock. the amygdalec
•
.::.:20 tomized and frontally lesioned subjects have
=
fewer "spontaneous gah"anic skin responses"
: during the shock sessions, suggesting an al
.,.1.2 tered base le\'el. So far. we have referred
.1-.4 .4'" 1.2·1.6 lJI·2.0
.A. SHOCI to phasic changes in the initial period of
(,bsen-ation. "'hich often reach asymptote
FIGL"RE4. Top: Curyes oj percentage of galvanic
\\"ithin three to five stimulus presentations.
skin response generated by three runs of stimuli
in ascending and descending intensity (in map) by However. while behm"ioral and some elec
the amygdaleclOmized (A~{) and control (X) trocortical responses appear to be normal
groups. Bottom: A finer breakdown oj stimulus during orienting, after frontal and amygdala
yalues from .I to 1.0 rnA. pooled ascending and
lesions (Bagshaw& Benzies. 1968;Schwartz
descending yalues. (From "Effect oj Amygdalec·
Lawn et a!.. 1961) the background Ine] of
tomy on Stimulus Threshold of the Monkey" by M.
H. Bagshaw and J. D. Pribram, Experimental these respoll5es is lo\\"er than for controls.
Nrwalop.\'. )963. 20. 197-202. Copyright 1968 by For example, ear flickir.g is practically ab
Academic Press. Reprinted by permission.) sent during interstimulus internls (Bag
sha,,' & Benzies. 1968). and while electro
their initiation (Fuller, Rosvold, & Pribram, myographic respnnses (lCCUr with normal
1957). latency. the amplitude of these resp0nses is
uJnsiderabh" reduced (Pribram, Reitz. ~Ic­
SCIIsitivity and Registratioll Xeil. & 5p~vack. 1974).
The question arises as to the significance .-\ccompanying the reduction in baseline of
for the orienting reaction of the "isceroauto phasic responses. a striking tonic psycho
nomic components per se. The absence of physiological effect followed amygdalectomy.
visceroautonomic reactivity during orienting This was the finding of a paradoxically ele
could result simply from lowering the sensi yated basal heart rate (Bagshaw & Benzies,
tivity of the organism to stimulation. How 1%.>:t: Pribram et a!.. 1974). The paradox
ever.resectior.soffrontal cortex (Grueninger. has been clarified by experimental results
Kimble. Grueninger, & Levine. 1965) or of (,btained by Elliott" (Elliott, Bankart. &
the amygdala (Bagshaw and Coppock. 1968; Light. 1970) in which he found that novel
!\1cXeil, 1972) do not abolish galvanic skin input had little effect on tonic heart rate or
THE CONTROL OF ATTENTION 123
had an effect (deceleratory) opposite to ex visceroautonomic responses. By way of its
pectations. However, response factors and diffuse connections,thissystem is responsible
incentive factors (reinforcing consequences) for the more ubiquitous "arousal" responses
hadstrongacceleratingeffects. Thus,arousal, recorded throughout the brain concomitant
though it may produce a brief initial phasic with orienting. Forebrain control over this
acceleration (Obrist, Wood, &Perez-Reyes, corebrain arousal system ~s exerted by re
1965), leads more often to tonic heart rate ciprocal facilitatory and inhibitory circuits
deceleration, which is indicative ofactivation, centered on the amygdala. These circuits
a process detailed in the next section. In control the onset and duration of neural
short, the monkeys with absent arousal reac arousal much as they control the onset and
tions are consistent in showing an elevated duration of visceroautonomic and appetitive
tonic heart rate. As Elliott's data indicate, responses.
and as will be detailed in the last section Our interpretation of the relationship be
of this article, elevated tonic heart rate is tween the lack ofvisceroautonomic responses
manifest \\'hen the situation demands "ef to orienting and the failure to habituate be
fort" on the part of the organism. haviorally has been to suggest that a defi
The effects of amygdalectomy can be in ciency is produced in the more ubiquitous
terpreted as follows: Because the specific central mechanism by which organisms "reg
controls on arousal are removed, behavioral ister" input.. When such failure in registra
arousal fails to lead to the registration of the tion occurs, the organism's nervous system
situation by altering the neuronal model but is temporarily swamped by the arousing in
results in nonspecific defensive "effort" to put and reacts defensively to shut out all
cope with the situation. This defense reac further input and thus leads to automatisms.
tion is characterized by an attempt to shut This interpretation fits the clinical picture
off further input (see Pribram, 1969), and of the amnestic states (deja vu and jamais
is reflected in an elevated heart rate and vu) and the automatisms occurring during
other changes indicative of a lack of readi psychomotor seizures produced by epileptic
ness to respond meaningfully to the input. lesions in the region ofthe amygdala. There
Thus "effort" is manifest in the absence of is also considerable congruity between this
readiness. This interpretation is borne out interpretation and those of Mednick and
by the results of an experiment in which in Schulsinger (1968) and ofVenables (Gruze
fant kittens were raised in isolation. When lier &Venables. 1972) in their report of two
examined at the age of 6 months their classes (galvanic skin responders and non
visceroautonomic and endocrine reactivity in responders) of patients diagnosed as schizo
orienting experiments was essentially similar phrenic. However, the interpretation also
to that of amygdalectomized subjects: They suffers from the difficulties that plague un
had not learned to cope with situations and derstanding of these clinical syndromes:
thus showed. the "defensive" syndrome sug How do disturbances of registration in im
gestive of considerable "effort" (Konrad & "mediate awareness influence subsequent re
Bagshaw, 1,970). trieval? This will be discussed further in
the following sections.
Summary
Studies relating brain function and the VIGILANT ATTENTION. EFFORT, AND THE
orienting reaction to sensory input have CONTROL OF ACTIVATION
pointed to the presence of a system of The interaction between behaving organ
neurons responding to the amount 'of input isms and their environment is not one-sided.
to them by maintaining or incrementing The organism is not just a switchboard for
their activity. This core system of neurons incoming stimulation. Rather, the essence
extends from the spinal cord through the of behaving organisms is that they are spon
brainstem reticular formation, including hy taneously active, generating changes in the
pothalamic sites. and lies in close proximity environment often by way of highly pro
to those responsible for the engenderment of grammed, that is, serially ordered, responses
124 KARL H. PRIBRAM AND DrANE McGurr.;!'ESS
(Miller, Galanter, & Pribram, 1960; Pri minute-long changes in heart rate and "en
bram, 1960b, 1962, 1963, 1971). These or during" changes in background level. We
:ganizationsof behavior must involve the con shall call both of these "tonic" in the present
struction of neuronal models in at least two review, though it is possible that the shorter
'ways: (a) control of the somatomotor sys~ changes are related to activation while more
tem which effects the responses and (b) enduring leyels of heart rate reflect effort.)
feedback from the outcomes (reinforcing The CNV was originally proposed to re
consequences) of the behavior. Sherrington flect an e.,"pectancy developed when a specific
(1955),in discussing central representations, response was contingent on mvaiting the sec
framed the issue in terms of whether the ond of two stimuli. This would suggest that
organism is intending to do something about the CNV reflects another central event in
the stimulus variables in the situation. In dicating that an input is about to be matched
a review of the evidence Germana (1968, to the organism's neuronal model., However,
1969) suggested that an'y central representa other workers suggested that the negative
tion or "neuronal model" must include such 6hift in potential reflects intended motor ac
"demand" characteristics. Thus he proposes tivity (e.g., Kornhuber & Deecke, 1965;
that Pavlov's "What is it?" reaction (which Vaughan, Costa, & Ritter, 1968). Still
we have called "arousal," the registration of others (Weinberg, 1972; Donchin, Ger
input in awareness) may not occur unless brandt, Leifer, & Tucker, 1972) demon
there is also a "What's to be done?" reac strated that a CNV occurs whether or not
tion. As we shall see, our analysis would an overt motor or even a discriminative re
suggest that both reactions occur and that sponse is required, provided some set or ex
they can be distinguished: registering input, pectancy is built into the situation. Such
indicating "What is it?", and vigilant readi sets do, of course, demand postural motor
ness signaling"What'stobedone?" Strictly readiness. Weinberg (1972), for instance,
behavioral analyses have led to a similar dis has shown that in man the CNV continues
sociation. The early studies of Lawrence until feedback from the consequences of re
I
(1949. 1950) and the more recent work of inforcement of the response occurs, and sim
Broadbent and Gregory (reviewed by Broad ilar evidence has been obtained in monkeys
bent, 1971) are perhaps the best known in (Pribram, Spinelli, &Kamback, 1967). In
terms of independent manipulations of stim a review of the CNV literature, Tecce
ulus set and of response set. (1972) suggests that three types of negative
potentials interact depending upon the de
Contingent Negative Variation
mands of the experiment: (a) CNV due to
and Activation
expectant attentional processes; (b) the mo
The simplest situation which demands that tor readiness potential signaling intention to
responses become serially organized is one act; and (c) more or less "spontaneous"
in which two successive input signals are shifts whose occurrence cannot yet be at
separated by an interval. The first input tributed to specific task situations. Thisclas
signals the organism to become ready to sification though consonant with results from
make a response to the second which deter a series of studies (Donchin. Otto. Ger
mines the outcome. A large body of data brandt, &Pribram, 1971, 1973) does not in
has been gathered in this situation, using dicate the full diversity of the CNV. Re
slow changes in brain electrical activity such cordings were made from several cortical
as the contingent negative variation (CNV) locations under a variety of vigilance condi
(Walter, Cooper, Aldridge, McCallum, & tions. These studies showed that sites which
'Winter, 1964) and tonic changes in heart produced transcortical negative variations
rate. Lacey and Lacey (1970) have estab (TNVs) depended upon the type of vigilance
lished a correlation between the amplitude task. Thus, frontal TNVsare recorded only
of CKV and heart rate deceleration. (]. 1. early in a task and when the task is changed;
Laceyand B. C. Lacey, 1974,and Malmoand motor negative potentials are recorded only
Belanger, 1967, distinguish between their 1- in anticipation of the necessity to make an