Habituation

Habituation is a decrease in the strength of a behavioral
response that occurs when an initially novel eliciting stimulus
is repeatedly presented. When an animal encounters a new
stimulus it first responds with a series of orienting reflexes.
With repetition of the stimulus, if it is neither rewarding nor
noxious, the animal reduces and ultimately suppresses its
responses. Habituation is probably the most ubiquitous of
all forms of learning. Through habituation, animals and
humans learn to ignore stimuli that have lost novelty or
meaning, thus freeing themselves to attend to stimuli that are
important. Habituation is thought to be the first learning
process to emerge in human infants and is used to study the
development of intellectual processes such as attention,
perception and memory in the newborn.

The most complete analysis of habituation has been carried out by Vincent Castellucci, Irving Kupfermann, and Eric
Kandel at Columbia University. They studied an invertebrate, the marine snail Aplysia californica, which has a
simple nervous system containing only 10 e5 cells. Aplysia has a reflex for withdrawing its respiratory organ, the gill,
and its siphon (a small fleshy spout above the gill used to expel seawater and waste). The gill and siphon withdraw if
a mild tactile stimulus is delivered to the siphon. With repeated stimulation, this reflex withdrawal habituates. As we
shall see later, this response can also be sensitized and classically conditioned.

Whereas the neural circuit , or wiring diagram, of the flexion reflex in the cat is complex, that for gill withdrawal is
simple. The reflex has an important monosynaptic component consisting of a group of motor neurons that mediate
the behavior and a group of sensory neurons that synapse on the motor neurons. There are also several excitatory
and inhibitory interneurons upon which the sensory neurons converge and that in turn synapse on the motor neurons
(figure 1). In response to a novel stimulus, the sensory neurons generate large excitatory postsynaptic potentials in
the interneurons and motor cells. These excitatory postsynaptic potentials summate both temporally and spatially and
cause the motor cells to discharge strongly, leading to a brisk withdrawal of the gill. As the stimulus is repeatedly
presented, the synaptic potentials produced by the sensory neurons in the interneurons and in the motor cells become
progressively smaller; fewer action potentials are therefore generated in the motor cells, and the behavior is reduced.
Finally, the postsynaptic potentials generated by the sensory neurons become very small and fail to elicit action
potentials in the motor neurons, at which point no behavior is produced. The memory for habituation is stored as a
persistent reduction in the effectiveness of the synaptic connections between the sensory and motor neurons. This
reduction leads to a diminished behavioral response that lasts for several hours.

The decrease in synaptic transmission results, in part, from a prolonged shutting off (inactivation) of the Ca++
channel in the presynaptic terminal, leading to a decrease in Ca++ influx and a diminished output of chemical
transmitter. After the reflex is habituated, a tactile stimulus ot the skin still activates the sensory neurons, and an
action potential still propagates into the terminals of the neurons. However, because the Ca++ channels are partly
inactivated, less Ca++ flows into the terminals with each action potential. Transmitter release depends on the influx
of Ca++ into the terminals with each action potential, therefore less transmitter is released (figure 4-B). The Ca++ is
thought to function in transmitter release by allowing the vesicles that contain the transmitter to be mobilized into
release sites at active zones and to bind to the surface membrane there - a necessary step for exocytosis. Thus, in
this simple case, short-term memory for a learning task is due not to reverberating activity in a closed chain of
neurons, but to a functional, or plastic, change in the strength of a previously existing set of connections. This seems
to be a general mechanism of habituation since a similar process accounts for short-term habituation of escape
responses in crayfish and cockroaches.

What are the limits of this plasticity? How much can the effectiveness of a given synapse change and how long can
the change last? Memory can be either short term, lasting for minutes or hours, or long term, lasting for days, weeks,
or years. Can changes in synaptic effectiveness also give rise to long-term memory? Whereas a single training
session of 10 stimuli in Aplysia leads to short-term habituation that can last for hours, 4 or more repeated training
sessions produce long-term habituation that lasts up to 3 weeks. Castellucci, Thomas Carew, and Kandel have
compared the connections between the sensory neurons and the motor neurons in control animals with those in
animals examined at various times after they acquired long-term habituation. In the control animals, 90% of the
sensory neurons made electrophysiologically detectable connections onto the motor neurons (figure 2). In contrast,
both 1 day and 1 week after long-term habituation, the detectable connections with the motor cells were reduced to
30%; the rest of the connections had been inactivated to such a degree that they could not be demonstrated with
electrophysiological techniques.

Thus, short and long term changes in synaptic efficacy can underlie certain instances of short and long term memory.
Moreover, this plastic capability is quite specific to a particular set of synapses. Most synaptic connections in the
nervous system of Aplysia are not at all affected by a pattern of stimulation that leads to the learning of habituation.
However, at a crucial synapse such as that identified in the withdrawal reflex - a synapse that has evolved to mediate
the consequences of experience and learning - a relatively small amount of stimulation can produce long-term changes
in synaptic strength.