Does the Olfactory System Modulate Affective Behavior in the Pigeon?*

Abstract

On the basis of his knowledge of the patterns of evolutionary development of the olfactory system and other forebrain structures, Herrick' proposed that the olfactory cortex served an activating function for "all cortical activities." In recent years, without addressing Herrick's proposal directly, several investigators have provided evidence that is pertinent to it. In an extensive review of this topic, Wenzell concluded that a number of behaviors are altered by a greatly diminished olfactory input and that this effect is not readily explicable in terms of perceptual loss alone. One of the principal themes emerging from this review is the apparent lack of influence on the cognitive or problem-solving aspect of behavior, as compared with the motivational or affective aspect. Regardless of the species being studied, after reducing or removing olfactory input it is typical to find significant changes occurring in such characteristics as reactivity to handling, aggression, and shock-avoidance learning. By contrast, relatively little effect is reported for such tasks as lever pressing with different schedules of food reinforcement or complex visual discriminations reinforced by food.Because so much of this work has been done with rodents, a group of animals for which olfactory signals are of notable importance, it is difficult to determine the degree to which reduced olfactory input represents a loss of specific information rather than a more general effect. For this reason, we have chosen to work exclusively with the pigeon so that the contaminating influence of the cue value of olfaction can be minimized. Although good evidence exists3 that pigeons rely to some extent on olfactory cues for guidance in homing, no other segment of their behavior has as yet been shown to depend directly on odorous information. In addition to this fundamental advantage, the pigeon also presents a distinct anatomical advantage in the ease with which the olfactory nerve fibers can be completely sectioned as compared with the rat, for example, in which such an operation is much more problematic. In a series of reports beginning in 1968,4-6 several types of behavior in the pigeon were shown to be affected by bilateral removal of the olfactory bulbs or bilateral section of the olfactory nerves. No effect on the behaviors in question was observed following the control operation of unilateral removal of a superficial piece of the hyperstriatum dorsale approximately equal in size to that of the olfactory bulbs.

Considerations on the role of olfactory input in avian navigation

“…An activating effect of odors is supported by recent neurobiological studies which indicated an activation of neurons in the hippocampal formation and of the navigation circuity by lateralized activation of neurons in the piriform cortex (Jorge et al, 2014(Jorge et al, , 2016. However, some older findings could also be interpreted in view of an activating role of odors, as they revealed effects of olfactory deprivation on tasks not involving odors, such as tonic immobility and optokinetic nystagmus (rhythmic movements) (Wenzel and Rausch, 1977;Dornfeld and Bilo, 1990) as well as responses to visual stimuli (Wenzel and Salzman, 1968). Even the strongly disruptive effect of irregularly changing magnetic fields on pigeon orientation was suppressed in birds that had been deprived of odors by being kept in purified air during its application (Wallraff et al, 1986).…”

The underestimated role of olfaction in avian reproduction?

“…In several experiments, Wenzel and collaborators were able to demonstrate, by a lesion approach, these non-olfactory functions of the olfactory pathway. After lesions of the olfactory nerves and/or bulbs, performance was significantly decreased in learning situations [48, 112] and changes in tonic immobility, aggression [114] and reactivity in new situations [115] were also detected.…”

Pheromones in birds: myth or reality?

“…However, it is known that, besides their role in the perception of olfactory stimuli, olfactory bulbs play a relatively complex role in behavioral arousal. The behavioral deficits observed following olfactory nerves sections (which results in a retrograde degeneration of the olfactory bulbs) could thus have been related to general effects on arousal independently of the perception of olfactory stimuli (Kenshalo and Isaac 1977) as observed repeatedly in behavioral studies of birds (Wenzel and Salzman 1968; Wenzel et al 1969; Hutton et al 1974; Wenzel and Rausch 1977). Available data do not permit to discriminate between these two interpretations but the second one appears, at present, less likely because other behaviors that are not directly linked to copulations such as aggressive behaviors were not affected (Fig.…”