both at the National Eye Institute in Bethesda, 

 Maryland, had already shown that in the visual sys- 

 tem, attention enhances the response of neurons to 

 stimuli. One neural pathway that seemed to play a 

 key role in paying attention to a stimulus was medi- 

 ated by the neurotransmitter dopamine — in other 

 words, the signals transmitted across synapses from 

 one neuron to the next along the pathway were 

 modulated by dopamine. The neurons that make 

 dopamine are clustered in the midbrain; their 

 axons — the long projections from the main body of 

 the nerve cell — send signals to a number of sites in 

 the brain, including the hippocampus. 



That suggested an obvious experiment. What 

 would happen to the spatial map of an animal that 

 was paying attention to its surroundings if dopamine 



pretty things, metallic things, words, blows, blood." 



By contrast, voluntary attention, such as paying 

 attention to where staff members sit in a new of- 

 fice environment, is a feature of explicit memory. 

 It arises from the need to process stimuli that are 

 not automatically salient to the nervous system. 

 James argued that voluntary attention is obviously 

 a conscious process in people; therefore, it is likely 

 to be initiated in the cerebral cortex. 



The molecular studies my colleagues and I have 

 conducted in Aplysia and mice support James's 

 contention that both forms of attention exist. In 

 both voluntary and involuntary attention, the short- 

 term memory of a salient stimulus is converted to 

 long-term memory through the activation of genes. 



was blocked from reaching its hippocampus? My 

 co-workers and I proved just what we had been led 

 to expect: Without dopamine, the spatial map in 

 the mice would not stabilize; the place cells in the 

 mice would not reliably fire as they did when the 

 spatial memory was fixed. Conversely, when we ac- 

 tivated dopamine receptors in the hippocampus, the 

 spatial map of an animal became more stable even 

 when the animal was not paying attention. 



In The Principles of Psychology, James pointed out 

 that there are at least two forms of attention: invol- 

 untary and voluntary. Involuntary attention is sup- 

 ported by automatic neural processes, and it is par- 

 ticularly evident in implicit memory. In classical 

 conditioning, for instance, animals learn to associate 

 two stimuli if and only if the conditioned stimulus is 

 salient or surprising. In the textbook case, a bell 

 rings when food is presented to a dog. After several 

 such training cycles, the sound of the bell alone — 

 the conditioned stimulus — is enough to get the dog 

 to salivate. Involuntary attention is activated by a 

 property of the external world — of the stimulus — 

 and it is captured, according to James, by "strange 

 things, moving things, wild animals, bright things, 



In both cases, neurological pathways and chemical 

 transmitters act as modulators, carrying a signal that 

 marks the stimulus for special attention. In response 

 to that signal, genes are turned on and proteins are 

 produced and sent to all the synapses to strengthen 

 the connections between neurons. 



For example, Aplysia normally withdraws its deli- 

 cate gill into its mantle cavity if its siphon is touched. 

 The response weakens, through habituation, if the 

 siphon is touched repeatedly but weakly. But if the 

 weak touch is then paired, through conditioning, 

 with a shock to the animal's tail, the weak touch 

 alone will stimulate a brisk response. The shock 

 causes the neurotransmitter serotonin to be released 

 along the neural pathway that carries out the effec- 

 tive motor response for withdrawing the gill. The 

 serotonin triggers protein kinase A, which turns on 

 genes that send structural proteins to the synapses 

 most relevant for quickly withdrawing the gill. Sim- 

 ilarly, when a mouse learns the spatial task that 

 switches off obnoxious lights and sounds, we pre- 

 sume that dopamine is released along the neural 

 pathways that represent the mouse's spati.il map. The 

 dopamine then triggers the production of protein 



March 2006 NATUR/W HISTORY 



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