Olfactory Imprinting of Amino Acids in Lacustrine Sockeye Salmon

Abstract

Juvenile salmon have an olfactory ability to imprint their natal stream odors, but neither the odor properties of natal stream water nor the imprinting timing and duration have been clarified as yet. Here we show, using electrophysiological and behavioral experiments, that one-year-old lacustrine sockeye salmon (Oncorhynchus nerka) can be imprinted around the stage of parr-smolt transformation (PST) by a single amino acid, 1 µM L-proline (Pro), or L-glutamic acid (Glu). We also show by real-time PCR that changes occur in mRNA levels of the salmon olfactory imprinting-related gene (SOIG) around PST. The electro-olfactogram (EOG) responses of test fish exposed to Pro in March (before PST) and April–June (during PST) for 2 weeks were significantly (1.7-fold) greater than those of non-exposed control fish, but not those of test fish exposed in July (after PST). When Pro and control water were added to the water inlets of a two-choice test tank during the spawning season 2 years after the test water exposure, 80% of maturing and matured test fish exposed before and during PST showed a preference for Pro, whereas those exposed after PST did not. The EOG response of test fish exposed to Pro or Glu for 1 hour, 6 hours, 1 day, 7 days, or 14 days in May revealed that only the response after 14 days of exposure was significantly (1.8-fold) greater than the control. The expression levels of SOIG mRNA increased before and during PST, and decreased after PST. We conclude that one-year-old lacustrine sockeye salmon can be imprinted by a single amino acid before and during PST, and that imprinting requires exposure for at least 14 days.

Effects of aggressive interaction on downstream movement and olfactory function in masu salmon, Oncorhynchus masou

“…Yamamoto et al (2010) also observed that the expression of SOIG mRNA in one-year-old sockeye salmon increased from March to June and decreased in July. The significantly different expression levels of SOIG mRNA in the OE between winners and losers were detected one week after the fighting contest, but not two hours after the contest.…”

Aluminum exposure impacts brain plasticity and behavior in Atlantic salmon (Salmo salar)

“…Furthermore, it is possible that the reduced forebrain neural plasticity and cognitive deficit at the critical smolt stage also affect imprinting, by altering the olfactory-telencephalic plasticity associated with smoltification (Ebbesson et al, 1996a;Ebbesson et al, 2003;Folgueira et al, 2004). Memories of the natal stream formed during imprinting are later used to return as adults (Hasler and Scholz, 1983;Yamamoto et al, 2010), and thus impaired imprinting could have a profound impact on return success. Such behavioral processes are likely to involve the area of the brain involved in spatial learning and memory, namely the dorsolateral area of the telencephalon (Ebbesson and Braithwaite, 2012).…”

“…With the addition of our data on behavioral impairment and decreased neural plasticity, a decrease in cognitive ability suggests that the impact of Al toxicity is playing a negative role, causing distress in the exposed fish. These kinds of negative effects may have consequences for the ability of smolts to imprint on their natal streams (Yamamoto et al, 2010); it has been established that the parr-smolt transformation is a critical period for neural development, including cell differentiation and proliferation (Ebbesson et al, 1996b;Ebbesson et al, 2003;Ebbesson et al, 2007;Ebbesson et al, 2011). Olfactory imprinted memory is formed during smolting and the loss of neural plasticity could therefore impair the ability of Atlantic salmon to return to their natal stream (Dittman et al, 1996).…”

Physiological Mechanisms of Imprinting and Homing Migration of Pacific Salmon

“…The olfactory receptor cells of coho salmon that had been imprinted with PEA had a higher sensitivity to PEA compared with non-imprinted fish (Nevitt et al 1994), and only fish that were exposed to PEA or natural stream odors during smoltification formed an imprinted memory . Using electrophysiological and behavioral experiments, Yamamoto et al (2010) have revealed that 1-year-old lacustrine sockeye salmon can be imprinted at smoltification by a single amino acid, 1 mM L-proline (Pro) or L-glutamic acid (Glu). The EOG responses of test fish exposed to Pro in March (before smoltification) and April-June (during smoltification) for 2 weeks were significantly greater than those of non-exposed control fish, but not those of test fish exposed in July (after smoltification).…”