Professional Documents
Culture Documents
Emotions and
the Aging Brain
Regrets and Remedies
I. I N T R O D U C T I O N
1990; Panksepp, 1982, 1985a, 1991, in press). We will use the convention
of labeling these systems by simple emotional terms, capitalized to high-
light that they do not just designate the garden-varieties of emotional
feelings, but also the neurological bases of such feelings. These include
neural circuits that mediate separation distress and sorrow (the PANIC
system), ones that mediate playfulness and joy (the PLAY system), ones
that control sexual desires and pleasures (the LUST systems), and ones
for maternal (or parental) nurturance and social b o n d i n g (the ACCEP-
TANCE system). There may be others, such as a system for social DOMI-
NANCE, but because it is debatable whether these are distinct from the
others mentioned, we will not discuss them as separate systems.
All of those listed above are based in the extended limbic areas of the
brain, as defined by MacLean (1990). In addition, there are the more
cold-blooded, reptilian emotional systems of FEAR and RAGE, as well as
the ever powerful appetitive motivational system that mediates explor-
atory drives and foraging behavior (which we have previously called the
Expectancy System but will henceforth term the SEEKING system).
Some of these, such as FEAR and RAGE, are closely intertwined and me-
diate, respectively, an organism's defense of bodily integrity and its re-
sponse to irritations that thwart freedom of action and possession of re-
sources. The extensive and compelling neural evidence on how these
psychobehavioral systems function during early development has been
extensively discussed elsewhere (Panksepp, in press). In the present
chapter we would like to summarize how their sensitivities and respon-
sivities change in old age; because we cannot do so on the basis of avail-
able empirical evidence, we shall proceed more on the basis of rational
argumentation.
One general factor that complicates any life span analysis of brain
emotional systems is that a great deal of learning transpires, and many
habits are established, broken, and otherwise changed over time. Be-
cause of these fluxes, there is really no way to analyze the changing sensi-
tivities of emotional circuits by using behavioral means alone. One must
analyze the changing dynamics of the underlying neural systems using
anatomical and electrophysiological approaches, and those analyses have
started in earnest but without parallel behavioral data, so it is difficult to
relate those findings to psychological issues.
acute at an early age than they will b e c o m e later in life. The PANIC sys-
tem affords a good example, because cross-species c o m p a r i s o n shows that
activity in this system can vary as a function of the organism's relative n e e d
for care and protection. The n e u r o d y n a m i c s of the brain systems that gen-
erate separation calls (or distress vocalizations, DVs) vary markedly in
species d e p e n d i n g on their ecological circumstances and modes of social
bonding. For instance, herbivores that are born precocious (at a relatively
mature level of m o t o r d e v e l o p m e n t ) , such as guinea pigs, chickens, and
ducks, d e m o n s t r a t e separation distress on the first day of life and exhibit
a p r o l o n g e d inverted-U type of trajectory of separation calls that contin-
ues until p u b e r t y (Panksepp et al., in press; Pettijohn, 1979). Altricial an-
imals, such as most carnivores, including dogs, exhibit similar p r o l o n g e d
patterns of separation distress (Scott, Stewart, & DeGhett, 1973), but they
show a delay in exhibiting the e m o t i o n a l response (i.e., till eye o p e n i n g
and some m o t o r c o m p e t e n c e ) , because it makes little evolutionary sense
to exhibit such noisy behavior as DVs until one is sufficiently mature to
have some credible means to get out of harm's way. Thus, a l t h o u g h they
can obviously generate physical distress calls before their eyes open (for
example, when exposed to a cold e n v i r o n m e n t ) , true social separation
D V s - - n a m e l y those that occur even in a warm, soft, and n o n d a n g e r o u s
e n v i r o n m e n t - - d o not begin till a b o u t 3 weeks of life (Gurski, Davis, &
Scott, 1980). Once developed, these animals exhibit DVs well into puberty.
H u m a n babies tend to follow a similar p a t t e r n - - t h e e m o t i o n a l re-
sponse takes a while to mature, till a b o u t 8 months of age, w h e r e u p o n it
is evident for many years. Because h u m a n s are one of the most n e o t e n o u s
species on the face of the earth (i.e., we have a remarkably long child-
h o o d ) , we can also u n d e r s t a n d why strong feelings of loneliness can con-
tinue for a lifetime. On the o t h e r hand, rats, also born altricial like dogs
and h u m a n s , exhibit a b o u t an 8-day delay in the exhibition of true sepa-
ration calls, but then only emit t h e m for a short period of a week or two,
during which time they also d e m o n s t r a t e a brief period of true attach-
m e n t to their m o t h e r s and nest sites. These patterns p r e s u m a b l y reflect
the m a t u r a t i o n of certain brain systems, such as corticotropin-releasing
factor (CRF) systems, which are known to p r o m o t e this e m o t i o n a l re-
sponse (Panksepp, Normansell, H e r m a n , Bishop, & Crepeau, 1988).
However, for our purposes, the key question m i g h t be, what causes
this e m o t i o n a l response to decline in all species as a function of matura-
tion? We can be fairly certain that the most obvious explanation is not
applicable to the case: The DV circuitry itself does not degrade, because
one can electrically stimulate the diencephalic and mesencephalic trajec-
tories of the system to re-evoke infantile separation calls even when ma-
ture animals no longer a p p e a r to use this response system in their natural
behavioral repertoire ( H e r m a n & Panksepp, 1981). One obvious alterna-
8 Jaak Panksepp and Anesa Miller
B. P L A Y and D O M I N A N C E Systems
The development of PLAY also exhibits an inverted U-shaped func-
tion, whereby the intensity and frequency of rough-and-tumble activities
ESB-DVs from DORSOMEDIAL THALAMUS
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Figure 1. Average brain stimulation elicited distress vocalizations (DVs) in guinea pigs as
a function of age and gonadal status from two separate sites within separation distress cir-
cuitry (i.e., dorsomedial thalamus and preoptic area). Male and female animals were surgi-
cally p r e p a r e d at least 1 week before testing, and current-intensity curves were run during
the three points in early d e v e l o p m e n t - - l a t e "childhood," ( 7 - 1 0 weeks), late juvenile period
( 1 1 - 1 4 weeks), and early adulthood ( 1 5 - 1 8 weeks of age). The data depicted represent re-
sults for the highest current level, constant at all ages. Clearly, electrical stimulation of the
brain (ESB)-elicited DVs declined as a function of age, and the decline was decreased by go-
nadectomy in both males and females. These data indicate that the maturation of gonadal
h o r m o n e systems promotes a decline in the responsivity of the separation distress system of
the brain (Sahley & Panksepp, 1983).
10 Jaak Panksepp and Anesa Miller
diminishes as animals enter late "childhood" and even more as they pro-
ceed through puberty (Panksepp, 1993; Panksepp, Siviy, & Normansell,
1984). We do not know what controls this decline, even though, again,
testosterone is a participant, because it can reduce juvenile playfulness
(Panksepp, 1989). Because we assume that the underlying play circuits
are a major source of the joy that organisms experience in social inter-
actions, we have had some interest in seeing whether we might be able to
resurrect play in its declining days using neurochemical manipulations.
For a synopsis of that work, see section V.
Although there is little empirical evidence on the functions of play,
it is likely that this activity exercises the brain systems that mediate
various social skillsmfor instance, how to win or lose gracefully and how
to handle oneself in competitive situations. Thus, rough-and-tumble play
seems to be a source process for social dominance and submission,
which are social issues that do not undergo significant decline as a func-
tion of age. Indeed, it is possible that among primates, as an individual
grows older, dominance emerges as much from playful, mutually positive
and beneficial i n t e r c h a n g e m f r o m the establishment of friendships and
c o a l i t i o n s ~ a s from brute force and intimidation. Indeed, analysis of
dominance in primate societies suggests that elevations of brain sero-
tonin can promote dominance (Raleigh, McGuire, Brammer, Pollack, &
Yuwiler, 1991) but not simply through an increase in aggression. Rather,
the establishment of confident and positive social relationships with
other members of the group allows the individuals with pharmacologi-
cally elevated serotonin activity to prevail. In rat societies, the animals
that have exhibited the highest levels of friendly juvenile play also tend
to be dominant. (Adams & Boice, 1989). It seems that juvenile playful-
ness paves the way to dominance.
In this context, it is also noteworthy that most h u m a n societies have
provided outlets for the vigorous expressions of playful dominance urges,
including medieval jousting and m o d e r n sports. The respect that these
forms of stylized play enjoy from powerful elderly humans (especially
males), including administrators of our universities, not to mention the
members of the business community who wrangle to purchase sport fran-
chises, testifies to the importance of play-dominance circuits in h u m a n
affairs. Even when one's own natural ability to express those urges has
markedly diminished, the symbolic value of supporting sport events at-
tests to the continuing powerful role of such motivations in h u m a n af-
fairs. We suspect the attraction of those activities t h r o u g h o u t the life
span, especially in aging males, reflects the fact that the PLAY systems of
the brain, which inspire young animals to frolic in youth, are the progen-
itors of systems and abilities that help mediate dominance in adult social
CHAPTER 1 Emotions and the Aging Brain 11
systems. Even when the urge to frolic has diminished, the symbolic power
and status urges have not.
D. The A C C E I ~ A N C E System(s)
In addition to the brain systems discussed above, the emotion we
commonly call love is also closely related to the parental ACCEPTANCE sys-
tems. In all mammals, nurturance is mediated by distinct brain circuits
(Numan, 1988), but it is also remarkably susceptible to the influences
of various peripheral hormonal processes and learning (Krasnegor &
Bridges, 1990; Winberg & Kjellmer, 1994). How many distinct brain sys-
tems should actually be subsumed in this category remains in doubt, but
in lower animals the maternal components of nurturant behavior are be-
ing well delineated (Krasnegor & Bridges, 1990; Numan, 1988). In labo-
ratory rats nurturant tendency can be monitored simply via measures of
"sensitization" or "concaveation." These terms designate the induction of
maternal behaviors (nest building, pup retrieval, and hovering over the
pups) in virgin rats, both male and female, via prolonged exposure to rat
pups. Although males exhibit some nurturance (Brown, 1986), gener-
ally, mature females exhibit faster sensitization than males. Likewise,
during a brief period of life (perhaps corresponding to the most intense
"doll-play phase" of h u m a n children), juvenile rats exhibit a high level of
nurturance, with no major difference between males and females. How-
ever, with the onset of puberty and adulthood, sensitization proceeds
more slowly in males than females, although homosexual male rats re-
main as responsive as females (see Krasnegor & Bridges, 1990; Signoret,
Fabre-Nys, & Balthazart, 1994), suggesting that an adaptive value of this
phenotype may be to reduce reproduction and facilitate nurturance un-
der stressful circumstances.
CHAPTER 1 Emotions and the Aging Brain 13
G. T h e F E A R System
All m a m m a l s have a f u n d a m e n t a l FEAR system in the brain, which
courses between amygdaloid, medial hypothalamic, and central gray
areas of the m i d b r a i n (Panksepp, 1991). Manifestations of this system
e m e r g e during early h u m a n d e v e l o p m e n t and have been reasonably well
characterized. H u m a n babies are afraid of falling before they are afraid
of darkness, and they fear darkness before they fear snakes and other
scary animals (Gray, 1987). The ability to cope with fears also probably be-
comes ever m o r e efficient as organisms grow older, thanks largely to the
d e v e l o p m e n t of cognitive strategies (i.e., the buffering effect of repre-
sentations of the past and future). It is possible that older animals' in-
creasing ability to remove themselves from harm's way simply allows for
lower activation of the FEAR system as organisms mature. This disuse ef-
fect could also be r e p r e s e n t e d in the brain as a gradual weakening of the
synaptic connectivities and chemistries of the FEAR system, but that is
not an established fact.
Although we know almost n o t h i n g a b o u t changes in the FEAR system
as a function of aging, one i m p o r t a n t issue to be considered is the ability
of this system to also b e c o m e sensitized as a function of experience. T h e r e
is suggestive evidence that this occurs, as appears to take place in PTSD.
Fear sensitization can be evoked simply by electrically stimulating the
16 Jaak Panksepp and Anesa Miller
IV. B R A I N C H A N G E S IN O L D AGE
A. Neuroanatomical Issues
The various forms of neural deterioration that characterize aging are
an object of active study. The neuropathologies underlying the most se-
CHAPTER 1 Emotions and the Aging Brain 17
the quality of life for aging individuals. As we will see in the next section,
important progress is being made.
V. THE N E U R O C H E M I C A L F O U N T A I N S OF YOUTH:
SLOWING THE CHANGES OF OLD AGE
crease the life span, which has now been observed u n d e r various condi-
tions (Regelson et al., 1988).
Although our search for that fountain of youth has m e t with only
m o d e s t success, let us briefly summarize what we have done. A m o n g the
first p h a r m a c o l o g i c a l manipulations that we evaluated on play were drugs
that affect the major biogenic-amine s y s t e m s m n a m e l y those of serotonin,
n o r e p i n e p h r i n e , and d o p a m i n e - - a s well as those that affect brain opi-
oids. We f o u n d that we could marginally increase play with (a) low doses
of broadly acting serotonin-receptor antagonists such as methysergide,
(b) low doses of a p o m o r p h i n e that reduce brain d o p a m i n e activity, and
(c) low doses of opiate-receptor agonists such as m o r p h i n e (Panksepp
et al., 1984, 1987). Accordingly, we p r o c e e d e d to evaluate each of these,
as well as all combinations of these agents, to see if we could reinvigorate
playfulness when it was declining during late puberty. Unfortunately,
none of these agents alone nor in any combination restored playfulness
in young adults.
We have not given up the quest. One possibility we are presently eval-
uating is the recently identified e n d o g e n o u s c a n n a b a n o i d system of the
brain (Childers, Sexton, & Roy, 1993), and we have had some success in
restoring playfulness as rats age (Pruitt & Panksepp, 1995). Of course, it
remains possible that no n e u r o p h a r m a c o l o g i c a l agent shall ever restore
full juvenile playfulness. The decline in play may reflect a deterioration
of circuits that c a n n o t be resurrected no matter what we do, or it may
reflect the decline in the genetic expression of certain play chemistries
that c a n n o t be rejuvenated without great advances in our ability to ma-
nipulate genetic expression. Of course, we will continue the quest, for it
is a worthy journey.
VI. C L O S I N G R E M A R K S
ACKNOWLEDGMENTS
This work was supported in part National Institutes of Health (NIH) grant
R15 HD30387, and The Memorial Foundation for Lost Children, Bowling Green,
OH 43402.
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