Activational effects of odours on avian navigation

Abstract

The sensory basis of the navigational map remains one of the most important and intriguing questions in animal behaviour. In birds, odours have been hypothesized to provide the primary source of map information. Convincing tests have shown that experienced homing pigeons rely on map information obtained at sites where they are exposed to natural odours, even if subsequently released (without additional olfactory information) at a different site. These findings have been interpreted as support for the olfactory map hypothesis. Using this 'false-release-site' (FRS) approach, we compared the effects of exposure to natural odours with that of exposure to a series of artificial odours lacking spatial information. Our findings show that olfactory exposure to either natural or artificial odours at an FRS caused pigeons to rely on map information obtained at the FRS, even if subsequently released at the true-release site in the opposite direction from the home loft. Because artificial odours did not provide map information, however, the findings clearly demonstrate that olfactory exposure provides no navigational information to pigeons whatsoever; instead it activates an independent non-olfactory map system. This test decisively contradicts the olfactory map hypothesis, which predicts that olfactory cues are the primary source of navigational information used by birds.

Odours stimulate neuronal activity in the dorsolateral area of the hippocampal formation during path integration

“…In behavioural experiments, we confirmed previous findings from other laboratories (for a review, see [5]) showing that homing orientation was disrupted when pigeons were deprived of olfactory cues either during displacement to [7], or after arrival at [8], a release site. However, our behavioural experiments also showed that while pigeons exhibited homing orientation when they had access to natural odours, they also exhibited homing orientation when exposed to a fixed sequence of artificial odours that did not provide path integration or site-based map information [7,8].…”

“…This suggests that (i) not only vestibular and optic flow but also olfactory cues drive activity in the dorsal thalamic nucleus, and (ii) this nucleus exhibits a heightened response to olfactory stimuli during displacement to the release site when birds are attending to cues used for path integration. Importantly, the elevated activity is observed in response to both natural odours that could provide navigational and/or activational input, and to artificial odours that have been shown to provide only activational information [7,8]. Because the dorsal thalamic nucleus receives both optic flow and vestibular input, and because it sends projections to hippocampal regions [23], it is a good candidate for relaying the route-based information that reaches the dorsolateral areas of the hippocampal formation.…”

“…air deprived of odours) during the same period of time as controls. Because previous behavioural experiments have shown that the sequence of artificial odours used in the current experiments did not provide the birds with navigational information [7,8] (see earlier discussion), any effect of these artificial odours on neuronal activity in the dorsolateral area of the hippocampal formation is unlikely to be the result of their involvement in providing map information by means of path integration or map-based cues. At the same time, exposing the birds to comparable olfactory treatments during displacement and simulated displacement (i.e.…”

“…Immediately after arriving at the release site, all the groups were placed in purified air for 30 min. Eight minutes prior to releasing the birds, the nostrils of all pigeons were anaesthetized with a Xylocaine spray (for further details, see [8]). Then all pigeons were released in a single flock composed of one to two individuals from each group treatment plus four additional individuals with no treatment.…”

“…Olfactory information has also been proposed to be the basis of a gradient map [4,5] used by experienced birds to determine geographical position [6]. However, findings from behavioural experiments have challenged the idea that odours provide navigational map information, suggesting instead that unfamiliar odours activate brain areas involved in processing non-olfactory map cues [7,8] (i.e. the dorsolateral area of the hippocampal formation).…”