ORIENTING REFLEX HABITUATION

The orienting reflex (OR) is a complex response of the organism to a novel stimulus. It was discovered by Ivan Pavlov ([1927] 1960) as an interruption of ongoing activity by presentation of an unexpected stimulus (external inhibition). This inhibition of the ongoing activity, accompanied by somatic, vegetative, electroencephalographic, humoral, and sensory manifestations, was termed the "what-is-it reflex." The OR is a set of components contributing to optimize the conditions of stimulus perception. A sequence of ORs directed toward new aspects of the environment constitutes an exploratory behavior. The somatic components of the OR are represented by eye and head targeting movements, perking of ears, and sniffing. The vasoconstriction of peripheral vessels and vasodilation of vessels of the head, heart rate deceleration, and skin galvanic response (SGR) constitute vegetative OR components. Positron Emission Tomography has demonstrated enhancement of blood supply in different brain areas during sensory stimulation. The electroencephalographic manifestation of OR is characterized by negative steady potential shift that parallels a transition from slow-wave brain activity to high-frequency oscillations, demonstrating an enhancement of the arousal level (Lindsley, 1961). Humoral components of OR are represented by (-endorphin and acetylcholine released within brain tissues. The sensory components of OR are expressed in a lowering of sensory thresholds and increase of fusion frequency.

The repeated presentation of a stimulus results in a gradual decrement of OR components, called habituation. The process of habituation is stimulus-selective. That selectivity can be demonstrated with respect to elementary features (intensity, frequency, color, location, duration) as well as to complex aspects of stimuli (shape, accord, heteromodal structure). The habituation of the OR is also semantically selective, indicating a high level of abstraction in the OR control. In the process of habituation of OR, a neuronal model of the presented stimulus is elaborated in the brain. Any change of stimulus parameters with respect to the established neuronal model results in an elicitation of the OR. After a response to a novel stimulus, one sees the OR recover to a standard stimulus, a phenomenon called dishabituation. The OR is evoked by a mismatch signal resulting from the comparison of the presented stimulus with the established neuronal model. If the stimulus coincides with the neuronal model, no OR is generated. The neuronal model can be regarded as a multidimensional, self-adjustable filter shaped by a repeatedly presented stimulus. The magnitude of the OR depends on the degree of noncoincidence of the stimulus with the shape of the multidimensional filter. In accordance with the degree of spreading of excitation, local and generalized forms of ORs are distinguished. Short and long duration of excitation constitutes a basis for separation of phasic and tonic forms of ORs. In the process of habituation, tonic and generalized forms of OR are transformed into phasic and local ones (Sokolov, 1963).

The habituation of the OR can be studied using event-related potentials (ERPs) represented by a sequence of positive (P1, P2, P3) and negative (N1, N2) brain waves elicited by stimulus onset.

The computer-based isolation of separate ERPs evoked by rare stimuli demonstrates a partial habituation of vertex N1 that parallels the habituation of SGR. A novel stimulus results in an increase of N1 and evocation of SGR. Thus the stimulus deviating from the neuronal model triggers a modality-nonspecific negativity overlapping the stable part of N1 (Verbaten, 1988). The deviant stimuli following with short intervals among standard ones generate a modality-specific mismatch negativity overlapping N1-P2 components (Näätänen, 1990). The OR evoked by non-signal stimuli is termed involuntary OR. It differs from an OR evoked by signal stimuli, which is termed voluntary OR (Maltzman, 1985). The OR habituated to a nonsignal stimulus is recovered under the influence of verbal instruction announcing that the stimulus is a target of the response. Such an enhancement of an OR due to verbal instruction is lacking in patients with frontal lobe lesions, whereas their ORs to nonsignal stimuli remain intact (Luria, 1973).

The verbal instruction actualizes a memory trace of the target stimulus. The presented stimuli are matched against the memory trace. The match signal is evident in brain ERPs as a processing negativity overlapping N1-N2. The processing negativity is the greater the more closely the stimulus matches the memory trace, which is activated by verbal instruction (Näätänen, 1990). Similar enhancement of OR can be observed in the process of elaboration of conditioned reflexes. The nonsignal stimulus evoking no OR after habituation produces an OR again after its reinforcement. During conditioned reflex stabilization, OR is gradually extinguished, but more slowly than in response to a nonsignal stimulus. When a new nonreinforced differential stimulus is introduced into the experimental procedure, the OR is reestablished. The more difficult is the differentiation of signals, the greater the OR. Thus the magnitude and stability of ORs depend on novelty, significance, and task difficulty. Involuntary and voluntary ORs can be integrated within a common attentional process: A novel non-signal stimulus triggering an involuntary OR followed by a voluntary OR constitutes sustained attention.

The OR has its own reinforcement value and can be used as a reinforcement in the elaboration of conditioned ORs. The (-endorphin released by novel stimulus presentation plays a role of positive reinforcement in a search for novelty. The OR can contribute as an exploratory drive in selection of new combinations of memory traces during creative activity.

The OR at the neuronal level is represented by several populations of cells. The most important are novelty detectors, represented by pyramidal hippocampal cells characterized by universally extended receptive fields. Being activated by novel stimuli, these cells demonstrate stimulus-selective habituation that parallels the OR habituation at the macro level. Any change of input stimulus results in their spiking again. Thus a multidimensional neuronal model of a stimulus is formed at a single pyramidal neuron of the hippocampus. The selectivity of the neuronal model is determined by specific neocortical feature detectors extracting different properties of the input signal in parallel. The feature detectors characterized by stable responses converge on novelty detectors through plastic (modifiable) synapses. The plasticity of synapses on novelty detectors is dependent on hippocampal dentate granule cells. A set of excitations generated in selective feature detectors reach pyramidal and dentate cells in parallel. The dentate cells have synapses on pyramidal cells controlling the habituation process. The synapses of feature detectors constitute a map of features on a single novelty detector.

The neuronal model is represented on such a feature map by a specific pattern of synapses depressed by repeated stimulus presentations. The output signals of novelty detectors are fed to activating brainstem reticular formation neurons, generating an arousal reaction. The rest of the hippocampal pyramidal neurons are sameness detectors characterized by a background firing. A new stimulus results in an inhibition of their spiking. This inhibitory reaction is habituated by repeated stimulus presentation. The inhibitory response is evoked again by any stimulus change. The maximal firing rate is observed in sameness neurons under familiar surroundings. The output signals from sameness detectors are directed to inactivating reticular formation neurons, inducing drowsiness and sleep. The selective habituation of the pyramidal cell responses is based on the potentiation of synapses of dentate cells on pyramidal neurons. Under such potentiation of dentate synapses, the pyramidal cells stop responding to afferent stimuli. The injection of antibodies against hippocampal granule cells results in elimination of pyramidal cell habituation (Vinogradova, 1970).

Such are the neuronal mechanisms of involuntary OR habituation. The neuronal mechanisms of voluntary OR are more complex (see Figure 1). The stimuli analyzed by feature detectors are recorded by memory units of the association cortex. The verbal instruction, through semantic units with the participation of frontal lobe mechanisms, selects a set of memory units as a template. The match signal generated by memory units of the template is recorded as processing negativity. The match signal is addressed to novelty detectors, resulting in an enhancement of OR to significant stimuli. Through novelty detectors and sensitization of activating units, novel stimulus results in an electroencephalographic arousal correlated with sensitization of feature detectors and external inhibition of ongoing activity at the level of the command neurons. The repeated presentation of a stimulus switches on sameness neurons, which, with participation of inactivating units, induce lowering of the arousal level, expressed in drowsiness and sleep.

Bibliography

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Näätänen, R. (1990). The role of attention in auditory information processing as revealed by event-related potentials and other brain measures of cognitive function. Behavioral and Brain Sciences 13, 201-288.

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—— (1975). The neuronal mechanisms of the orienting reflex. In E. N. Sokolov and O. S. Vinogradova, eds., Neuronal mechanisms of the orienting reflex. Hillsdale, NJ: Erlbaum.

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Vinogradova, O. S. (1970). Registration of information and the limbic system. In G. Horn and R. Hind, eds., Short-term changes in neuronal activity and behavior. Cambridge, UK: Cambridge University Press.

E. N.Sokolov