Download Is there anything “autonomous” in the nervous system?

Adv Physiol Educ 30: 9 –12, 2006;
doi:10.1152/advan.00022.2005.
A Personal View
Is there anything “autonomous” in the nervous system?
Alberto A. Rasia-Filho
Fundação Faculdade Federal de Ciências Médicas, Department of Physiological Sciences (Physiology and Biophysics),
and Universidade Federal do Rio Grande do Sul, Postgraduation in Neuroscience, Porto Alegre, Brazil
Submitted 29 March 2005; accepted in final form 31 October 2005
sympathetic; parasympathetic; vegetative; homeostasis; visceral
THE TERMS “autonomous” or “autonomic” are commonly used
to identify one part of the nervous system that deals with
adjustments of widespread physiological variables needed for
maintenance of life and occurrence of behaviors. The so-called
“autonomic nervous system” (ANS) has been divided in two
broad parts: sympathetic and parasympathetic. In addition, a
third component has been included and is called the “enteric”
nervous system, which differs in structure and function from
the two foregoing divisions (2).
The definition found in dictionaries for autonomic refers to
something that has autonomy, self-government. Autonomy, by
its turn, is something that is independent (7, 25). However,
there is nothing in our whole indivisible body that is literally
independent, that works without being affected by any other
system or that can decide, by individual “desire,” when to
execute (or not) a given function. If so, imagine what a
coincidence it must be to behave as we normally do if all parts
of our organism were embodied with own “free will.” As
stated, “The autonomy of this part of the nervous system is
illusory, since it is intimately responsive to changes in somatic
activities” (2). All body systems are dependent and affected by
Address for reprint requests and other correspondence: A. A. RasiaFilho, Fundação Faculdade Federal de Ciências Médicas, Fisiologia, R.
Sarmento Leite 245, Porto Alegre RS 90050-170, Brazil (e-mail:
[email protected]).
the action of others in a multicellular organization. And this
dynamic relation is in the core of homeostasis, a fundamental
concept in physiology (4 – 6). Unfortunately, the term autonomic itself should not be even considered didatic, and, although it might be considered a “subtle” incorrectness and a
historical contribution, it is actually a conceptual mistake about
nervous organization (3).
When thinking of another nomenclature to be employed, the
second term usually used to describe the sympathetic, parasympathetic, and gastrointestinal tract neural components is
“vegetative.” For example, “vegetative nervous system,” “neurovegetative,” or “vegetative responses” are sometimes employed instead of ANS or autonomic responses. Notwithstanding, when looking for the meaning of vegetative, one is
addressed to something that is “involuntary or passive” (“like
the growth of plants”) or “showing little mental activity.”
Involuntary is something that is “not done of one’s own free
will, unintentional, accidental, not consciously controlled, automatic” (7, 25). Let us consider this definition further. The
effects of these neurons are not unintentional or passive or
involving little “mental” activity. And these terms are not
synonymous and do not imply the same as “not consciously
controlled” or “unconscious.” In sharp contrast with this definition, neural activities are intentionally activated for the
adequacy of the physiological variables according to the ongoing needs of the behaving animal. They are not merely
1043-4046/06 $8.00 Copyright © 2006 The American Physiological Society
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Rasia-Filho, Alberto A. Is there anything “autonomous” in the nervous system?
Adv Physiol Educ 30: 9 –12, 2006; doi:10.1152/advan.00022.2005.—The terms
“autonomous” or “vegetative” are currently used to identify one part of the nervous
system composed of sympathetic, parasympathetic, and gastrointestinal divisions.
However, the concepts that are under the literal meaning of these words can lead
to misconceptions about the actual nervous organization. Some clear-cut examples
indicate that no element shows “autonomy” in an integrated body. Nor are they
solely “passive” or generated “without mental elaboration.” In addition, to be ”not
consciously controlled“ is not a unique attribute of these components. Another term
that could be proposed is “homeostatic nervous system” for providing conditions to
the execution of behaviors and maintenance of the internal milieu within normal
ranges. But, not all homeostatic conditions are under the direct influence of these
groups of neurons, and some situations clearly impose different ranges for some
variables that are adaptative (or hazardous) in the tentative of successfully coping
with challenging situations. Finally, the name “nervous system for visceral control”
emerges as another possibility. Unfortunately, it is not only “viscera” that represent
end targets for this specific innervation. Therefore, it is commented that no quite
adequate term for the sympathetic, parasympathetic, and gastrointestinal divisions
has already been coined. The basic condition for a new term is that it should clearly
imply the whole integrated and collaborative functions that the components have in
an indivisible organism, including the neuroendocrine, immunological, and respiratory systems. Until that, we can call these parts simply by their own names and
avoid terms that are more “convenient” than appropriate.
A Personal View
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AUTONOMY IN THE NERVOUS SYSTEM?
that control blood pressure but also by reciprocal inhibitory
innervations in the heart wall (1, 15, 17, 22). “Both divisions
are tonically active and operate in conjunction with each other
and with somatic motor system to regulate most behavior, be it
normal or emergency. Although several visceral functions are
controlled predominantly by one or other division . . . it is the
balance of activity between the two that helps maintain an
internal stable environment in the face of changing external
conditions.” (14)
Indeed, these counteractions have to be emphasized because
it would be puzzling to find the general purpose for some
physiological variables changes when they are studied isolated.
Integrated, in the context of the need of an adequate behavior,
they are logically linked. An animal that is faced with a
threatening situation has to decide, among different strategies,
what is apparently the best choice for the conservation of its
life and, in a broad sense, of its species. For example, when
sympathetic activation occurs, cardiac output and systemic
blood flow increase and, whereas vasodilation occurs for increasing the blood supply to active skeletal muscles for posture
and intended movements, vasoconstrition in the skin can reduce blood loss in a region that is highly susceptible of
damage. A decreased time for blood clothing avoids a great
hemorrhage, and a higher sudoresis makes the skin moistened
and the animal difficult to be caught. At the same time, there is
enhanced breathing movements and airflow volume for gaseous changes and pH regulation. Liver glycogenolisis is stimulated, along with the mobilization of fatty acids from adipose
tissue. Muscular strength and muscle glycolysis are also improved and, for additional energy production, also occur with
higher oxygen-hemoglobin dissociation and oxygen delivery to
activated cells. Wave frequencies in the EEG increase, which
reflects diffuse neuronal activation, and mydriasis serves to
have more visual information and for deciding the best behavioral strategy to execute, such as skipping out of a dangerous
place. By the action of ␣-adrenergic receptors, the secretion of
insulin is inhibited (it would be useless to restore energy
reserves at this moment) and glucagon secretion is stimulated
by ␤-adrenergic receptors. Cortisol, as well as other stressrelated hormones, can be more released into the circulation,
and adrenal hormones can indirectly affect the consolidation of
memories. Cells of the immunological system, lymphoid tissues, and cytokines are also involved in this integrated response.
On the basis of these data and because these responses,
including the metabolic ones, can no longer be claimed literally
as autonomic or vegetative, it could be proposed a name of
nervous system for “homeostatic regulation.” This term would
incorporate the sympathetic, parasympathetic, and gastrointestinal divisions and correctly put together the cardiovascular,
respiratory (and its motor component for breathing), renal,
endocrine (with its neuroendocrine control), and hematological
systems for a common physiological purpose. “Our studies of
bodily homeostasis can then take place in a wider context.
Thus, in a study of fluid and electrolyte balance, observations
of behavioral strategies used to find water and salt in deficient
environments will take their place along with relevant hormonal and neural control of absorption and excretory mechanisms” (3). Moreover, dynamic fluctuations in the normal
range of functioning of this “homeostatic nervous system” are
quite possible, actively elaborated, and actually expected to
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passive ones or “side effects;” rather, they should represent the
best (or, sometimes, the possible) combination for the organic
variables at each moment. These homeostatic adjustments
(with the afferent and efferent pathways they involve) are
purposeful and organized concomitantly with behaviors to
provide basic conditions for their executions, including
those ones with no apparent somatic motor activity modifications (3, 23).
In addition, consciousness would not to be an epiphenomenon of neuroglial processing of information. Rather, it appears
to be an activity needed for data interpretation and for choice
decisions (24), although it is very likely that most of nervous
system function occurs without conscious awareness. If “not
consciously controlled” was considered as a need for being
considered vegetative, the neurochemical control of body
weight, basal ganglia implicit memories (10), and the perception of backwardly masked fearful faces by the amygdala (9)
should also be included in this same category (and they never
were indeed). Also, involuntary and clearly related with motor
acts are the spinal organization of the stretch reflex, the
proprioceptive afference to the cerebellum, or the active inhibition of most skeletal muscles when dreaming occurs (10).
This would serve to comment that the activity of sympathetic,
parasympathetic, and gastrointestinal divisions could not be
stated as the “involuntary motor system” as a proper, unique, or
ultimate characteristic of them. Furthermore, there is no “motor” activity in the relevant sympathetic innervation of the
kidney, adrenal medulla, and so on.
It is beyond doubt that some physiological variables are not
under complete voluntary control. For example, it could be said
that no one is able to greatly decrease one’s own heart rate and
blood pressure. This does not necessarily mean that volition
cannot affect them, because “biofeedback” training can provide useful adjunct results for the treatment of moderate
essential hypertension (26). Also well known are the changes
in cardiovascular variables related to voluntary motor acts or
associated with emotionally loaded situations, when these
changes are intended to help the animal better cope with the
situations. In this same regard, in the treatment for precocious
ejaculation or in some cases of male impotence, “mental”
activity has to occur for emission controlling or for conscious
awareness of the suspected “psychological” [that is “organic,”
by definition, because is happening in a body organ (19)] cause
of the dysfunction.
Therefore, let us see if another, better term can emerge from
functional evidences based on classical responses displayed by
the sympathetic and parasympathetic nervous systems. It is not
unusual to hear or read or sometimes it stays implicit that
actions of these divisions promote opposite effects in the
organs they innervate. However, for the precise aim of a
homeostatic response that requires effectiveness, energy economy and sometimes fast responses, the sympathetic and parasympathetic can be adjoined and collaborate for a final net
effect. The mobilization of physiological variables does not
occur in an all-or-none manner and is not exclusive of extreme
“fight or flight” conditions; rather, they can occur with graded
intensities in ordinarily daily situations (23). For instance, if
one needs to enhance blood pressure, a higher gain in the
response can be obtained with concomitant enhancement of
sympathetic activity and inhibition of parasympathetic activity.
This is obtained not only in the central nervous system areas
A Personal View
AUTONOMY IN THE NERVOUS SYSTEM?
ciated with anticipatory behavioral and physiological responses, and are vulnerable to physiological overload and the
breakdown of regulatory capacities (16, 20). It is the viability
of the internal milieu that is aimed toward when the needs
exceed the limiting capacity of the system. They can lead to
acute adaptations or to chronic situations and can have damaging side effects by imposing the establishment of different
ranges for some variables, as in the endocrine and immunological systems (21) or in obesity-related hypertension (12). On
the other hand, these adaptations would represent that “control
systems must be capable of radically reorganizing themselves
in response to long-term changes in circumstances . . . . called
ultrastability, the ability to maintain homeostasis not by local
hill climbing, small incremental changes in the model’s parameters, but by a sort of leap to a neighboring peak.” (for details,
see Ref. 5)
Finally, taking into account the end targets that are under
control, another term for the sympathetic, parasympathetic, and
gastrointestinal divisions could be suggested: “nervous system
for visceral control.” Accordingly, the sympathetic and parasympathetic systems innervate and form the “visceral (splanchnic) component of the nervous system” (2). It has already been
stated that “the autonomic nervous system is a visceral sensory
and motor system”. . . and . . .“visceral reflexes are not under
voluntary control, nor they impinge on consciousness, with few
exceptions” (14). From the above-mentioned statements, let us
remember that unconscious is not necessarily the same as
autonomic. And, whereas viscera means the “large internal
organs of the body,” it does not represent unique end targets for
this innervation. It is right that these neurons are found reaching and close to viscera, but it is also true that they can be
found in salivary glands, blood vessels, smooth muscle, adipocytes, mast cells, melanophores, interstitial cells, and motor
end plates (2, 13).
Regrettably, it was not possible to find a term that quite
satisfied the morphological and physiological characteristics of
the group of neurons in discussion. It is argued here that the
current terms for the sympathetic, parasympathetic, and gastrointestinal components of the nervous system are not completely adequate. Indeed, “what is in a name” and what does it
imply? It still deserves further academic debate to coin another
term with the formal obligation to include the characteristics of
the components it is naming and, in addition, to consider their
inseparable and parallel actions in the functional conjuncture of
one sole animal body. But, could the solution for this issue be
even easier? Maybe one can say yes. Instead of pursuing a
name that can be prone to objections, it could be simply left as
the sympathetic, parasympathetic, and gastrointestinal nervous
system, to call them by no less than what they really are, i.e.,
by their own names. More than an intellectual challenge to find
words that must congregate heterogeneous structures or that
can involuntarily hide some relevant aspects of their anatomic
and functional organization, this last possibility would be
accepted without great effort. And, most importantly, it shall
not serve to perpetuate names that are more “convenient” than
appropriate (2), even more when teaching to our students.
These students shall also learn the purposes of the integrated
actions of cells, tissues, and organs. For the reasons life is
based and life is for in dynamic organisms.
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occur. Ample and physiological variations can be found in
some parameters along time (e.g., those described as circadian
rhythms) or in certain sleep phases, after eating sustaining
food, or even in the early days of babyhood. Being repetitive
and under normal situations, a healthy body should bear the
brunt of them safely during certain periods of time. Obviously,
some events can be out of control and lead to serious health
hazards; but, should these changes always be harmful to an
animal whenever it is faced with a new situation, probably then
ours and other species would not be here. Cannon (4), in his
book The Wisdom of the Body, addressed this topic: “In 1907,
Metzer, in an important and suggestive paper, drew attention to
a group of facts which he had gathered to throw light on the
question whether our bodies are organized on a generous or on
a narrowly limited plan. He pointed out that when an engineer
estimates the weights which a bridge or beam must support, or
the pressures to which a boiler will be subjected, he does not
provide merely for those stresses in building the structure. The
engineer multiplies his estimates by three, six or even by
twenty, in order to make the structure thoroughly reliable. The
greater strength of the material, above that calculated as necessary, measures what is known as a “factor of safety.”
Nevertheless, it could be argued that not all homeostatic
conditions are under the strict control of the sympathetic,
parasympathetic, or gastrointestinal nervous system. For example, homeostatic control also includes the regulation of
plasmatic electrolytic, pH, and gaseous composition. Although
there are relevant sympathetic afferences to the kidneys (8), the
ultimate maintenance of homeostatic levels of Na⫹ and K⫹ in
the circulation is not directly or solely an effect mediated by
renal cathecolamines. An animal with destruction of the sympathetic nervous system is unable to normally respond to
variations of hidric and electrolytic balance (13). However, this
division is not essential to life when the animal is living in a
controlled environment because, fundamentally, each different
tissue possesses the ability to autoregulate local blood flow to
ensure normal short-term and long-term functioning based on
metabolic and functional needs (11). Likewise, some behaviors can be programmed and executed to correct or maintain
variables within normal ranges. But, for the proper execution of some behaviors or due to them, some reflex responses can be “bypassed,” and homeostatic adjustments
found in resting can became intentionally inhibited or temporarily adjusted by hierarquical reasons of importance.
That is, exercise or defense reactions are accompanied by a
programmed decrease of the baroreceptor reflex-related cardiovascular response, increased breathing amplitude can
occur in awake and behaving animals due to the inhibition
of the Hering-Breuer inflation reflex (23), thermoregulatory
responses to environmental thermal loads are suppressed
during paradoxal sleep (18), and thirst ceases immediately
after an animal drinks water, several minutes before blood
osmolarity is restored to a lower value (23).
Animals might also have to achieve stability of their variables through changes of state related to challenging circumstances. In this sense, the concept of “allostasis” (allo, meaning
different, and stasis, meaning constancy, i.e., “achieving stability through change”) was introduced to take into account
regulatory systems that develop variable set points of control,
show individual differences in expression according with the
capacity of the animal to cope with new situations, are asso-
11
A Personal View
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AUTONOMY IN THE NERVOUS SYSTEM?
ACKNOWLEDGMENTS
Author remains deeply indebted to Dr. Cesar Timo-Iaria (in memoriam) for
his incentive and valuable conceptual comments added in the present version
of this manuscript. The author is also grateful to Drs. Katya Rigatto and Pedro
Dall’Ago (Fundação Faculdade Federal de Ciências Médicas) for their opinions and suggestions on this work.
14.
15.
GRANTS
A. A. Rasa-Filho is a Conselho Nacional de Desenvolvimento Cientı́fico e
Tecnológico investigator.
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