Anderson's neural reuse hypothesis posits the development of functional overlap in brain system circuits to accommodate increasingly complex and evolutionarily more advanced functions. The notion of reuse is also consistent with many researchers' thinking regarding multiple functions of brain circuitry. The work in our laboratory centers around the ongoing processes of cognitive functions during sleep, and its various stages, that might be associated with different forms of memory, including implicit, explicit, and emotional salient memories with specific yet overlapping or instantiated neural circuits associated with each. Yet we operate with the implied assumption that memory is not the sole function of sleep, but an evolutionary epiphenomena that has played a central role in the development and retention of complex and advanced cognitive abilities.
Species adaptation of the basic rest-activity cycle seen in plants and animals suggest an evolutionary adaptive aspect to this universal behavior. The development of this universal process appears to fulfill a myriad of ancillary activities. There has certainly been much debate about the functional purpose of sleep – the rest aspect of the rest-activity cycle. While there is no debate about the functional importance of eating, drinking, and engaging in sexual behavior, a clear conclusion regarding the biological state of sleep has yet to be determined. Many theories abound, and memory consolidation is one such theory. Although sleep is more likely to be an adaptive state for more vital purposes such as energy conservation, the sleeping state depends upon essential neural circuitry that hosts neurophysiological and neurochemical dynamics important for memory processing. One such example, the cortical cycle of synchronized and desynchronized neural firing during slow wave sleep (SWS) may serve to globally reduce and restrict unsustainable synaptic growth resultant of learning experiences in wakefulness (Tononi & Cirelli Reference Tononi and Cirelli2003; Reference Tononi and Cirelli2006). At the same time, the reduction of weak synaptic connection may inadvertently enhance the signal-to-noise ratio for more significant connections that are strong enough to survive this global downscaling. Another example might be the neurophysiological and neurochemical dynamics occurring during the various stages of sleep, involving brainstem activation or hippocampal to cortical off-line activation (Buszáki Reference Buszáki1998; Hasselmo Reference Hasselmo1999), acting upon newly acquired information, thereby facilitating long-term memory consolidation.
Several laboratories, including our own (Alger et al. Reference Alger, Lau and Fishbein2010; Tucker et al. Reference Tucker, Hirota, Wamsley, Lau, Chaklader and Fishbein2006), have provided evidence demonstrating that the neurobiological state of sleep plays an essential role in facilitating the formation of direct associative and non-associative memories. We (Lau et al. Reference Lau, Tucker and Fishbein2010), along with Wagner et al. (Reference Wagner, Gais, Haider, Verleger and Born2004), Ellenbogen et al. (Reference Ellenbogen, Hu, Payne, Titone and Walker2007), and Payne et al. (Reference Payne, Schacter, Propper, Huang, Wamsley, Tucker, Walker and Stickgold2009), have extended these findings demonstrating that sleep also facilitates the formation of relational memories – the flexible representation and expression of items not directly learned. The mechanisms underlying the processing of direct associative and relational memory appear related to the physiological events occurring during SWS (Lau et al. Reference Lau, Tucker and Fishbein2010). Besides temporally coordinated physiological activities specific to the hippocampal-neocortical circuitry (Buszáki Reference Buszáki1998), SWS is also characterized by global synchronized oscillatory activities (Tononi & Cirelli Reference Tononi and Cirelli2003; Reference Tononi and Cirelli2006) and depressed acetylcholine level (Hasselmo Reference Hasselmo1999). Perhaps associations between items learned before sleep are strengthened and reorganized inadvertently through these widespread activities during sleep to form more energy-efficient and functionally flexible networks among existing neural substrates.
Similarly, once treated as distinct and separate from that of cognition, emotions involve neural circuitry that host neurophysiological and neurochemical dynamics. The traditional limbic system theory supports the idea that neural resources (e.g., physiological or somatic) were carried out by the evolutionarily old cortex (i.e., the so-called reptilian brain), whereas cognitive processes (i.e., higher-order functions) were subserved by the neocortex. The present view, however, integrates both the limbic system and the neocortex as separate but interacting brain systems functioning in parallel. The processes of long-term potentiation (LTP), long-term depression (LTD), and neural plasticity are just some of the ways that the brain can reorganize and change its pattern of activity across cortical regions (and across modalities) in response to experiences.
Following this logic, one can imagine that neural reuse, whether evolutionary old or new, also follows a similar trend whereby mental functions are mediated by separate but interdependent brain processes. In the context of emotional arousal, the domain highly implicated for such processing is the amygdala, interacting with the hippocampus, thereby playing a role in supporting the formation and storage of emotionally salient forms of declarative memories. The brain state supporting such a process appears to occur primarily during the low-voltage, fast activity of rapid eye movement (REM) and stage II sleep (DeJesús et al., in preparation).
Therefore, the processes ongoing during the different sleep stages, stage II, SWS and REM sleep, might serve to consolidate distinct aspects of emotionally salient declarative memories. Whether it is one process or mechanism or another, it would appear that evolutionary adaptation evolved neural circuits that may have been exploited for different uses, and one such use may be the cognitive processes engaged in memory consolidation that occur during the neurobiological states of sleep.
Therefore, the notion of neural reuse should not be limited to recycling of neural circuitry, but should extend to recycling of neurobiological processes that may have well served the evolutionary advancement in mammalian intelligence.
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Anderson's neural reuse hypothesis posits the development of functional overlap in brain system circuits to accommodate increasingly complex and evolutionarily more advanced functions. The notion of reuse is also consistent with many researchers' thinking regarding multiple functions of brain circuitry. The work in our laboratory centers around the ongoing processes of cognitive functions during sleep, and its various stages, that might be associated with different forms of memory, including implicit, explicit, and emotional salient memories with specific yet overlapping or instantiated neural circuits associated with each. Yet we operate with the implied assumption that memory is not the sole function of sleep, but an evolutionary epiphenomena that has played a central role in the development and retention of complex and advanced cognitive abilities.
Species adaptation of the basic rest-activity cycle seen in plants and animals suggest an evolutionary adaptive aspect to this universal behavior. The development of this universal process appears to fulfill a myriad of ancillary activities. There has certainly been much debate about the functional purpose of sleep – the rest aspect of the rest-activity cycle. While there is no debate about the functional importance of eating, drinking, and engaging in sexual behavior, a clear conclusion regarding the biological state of sleep has yet to be determined. Many theories abound, and memory consolidation is one such theory. Although sleep is more likely to be an adaptive state for more vital purposes such as energy conservation, the sleeping state depends upon essential neural circuitry that hosts neurophysiological and neurochemical dynamics important for memory processing. One such example, the cortical cycle of synchronized and desynchronized neural firing during slow wave sleep (SWS) may serve to globally reduce and restrict unsustainable synaptic growth resultant of learning experiences in wakefulness (Tononi & Cirelli Reference Tononi and Cirelli2003; Reference Tononi and Cirelli2006). At the same time, the reduction of weak synaptic connection may inadvertently enhance the signal-to-noise ratio for more significant connections that are strong enough to survive this global downscaling. Another example might be the neurophysiological and neurochemical dynamics occurring during the various stages of sleep, involving brainstem activation or hippocampal to cortical off-line activation (Buszáki Reference Buszáki1998; Hasselmo Reference Hasselmo1999), acting upon newly acquired information, thereby facilitating long-term memory consolidation.
Several laboratories, including our own (Alger et al. Reference Alger, Lau and Fishbein2010; Tucker et al. Reference Tucker, Hirota, Wamsley, Lau, Chaklader and Fishbein2006), have provided evidence demonstrating that the neurobiological state of sleep plays an essential role in facilitating the formation of direct associative and non-associative memories. We (Lau et al. Reference Lau, Tucker and Fishbein2010), along with Wagner et al. (Reference Wagner, Gais, Haider, Verleger and Born2004), Ellenbogen et al. (Reference Ellenbogen, Hu, Payne, Titone and Walker2007), and Payne et al. (Reference Payne, Schacter, Propper, Huang, Wamsley, Tucker, Walker and Stickgold2009), have extended these findings demonstrating that sleep also facilitates the formation of relational memories – the flexible representation and expression of items not directly learned. The mechanisms underlying the processing of direct associative and relational memory appear related to the physiological events occurring during SWS (Lau et al. Reference Lau, Tucker and Fishbein2010). Besides temporally coordinated physiological activities specific to the hippocampal-neocortical circuitry (Buszáki Reference Buszáki1998), SWS is also characterized by global synchronized oscillatory activities (Tononi & Cirelli Reference Tononi and Cirelli2003; Reference Tononi and Cirelli2006) and depressed acetylcholine level (Hasselmo Reference Hasselmo1999). Perhaps associations between items learned before sleep are strengthened and reorganized inadvertently through these widespread activities during sleep to form more energy-efficient and functionally flexible networks among existing neural substrates.
Similarly, once treated as distinct and separate from that of cognition, emotions involve neural circuitry that host neurophysiological and neurochemical dynamics. The traditional limbic system theory supports the idea that neural resources (e.g., physiological or somatic) were carried out by the evolutionarily old cortex (i.e., the so-called reptilian brain), whereas cognitive processes (i.e., higher-order functions) were subserved by the neocortex. The present view, however, integrates both the limbic system and the neocortex as separate but interacting brain systems functioning in parallel. The processes of long-term potentiation (LTP), long-term depression (LTD), and neural plasticity are just some of the ways that the brain can reorganize and change its pattern of activity across cortical regions (and across modalities) in response to experiences.
Following this logic, one can imagine that neural reuse, whether evolutionary old or new, also follows a similar trend whereby mental functions are mediated by separate but interdependent brain processes. In the context of emotional arousal, the domain highly implicated for such processing is the amygdala, interacting with the hippocampus, thereby playing a role in supporting the formation and storage of emotionally salient forms of declarative memories. The brain state supporting such a process appears to occur primarily during the low-voltage, fast activity of rapid eye movement (REM) and stage II sleep (DeJesús et al., in preparation).
Therefore, the processes ongoing during the different sleep stages, stage II, SWS and REM sleep, might serve to consolidate distinct aspects of emotionally salient declarative memories. Whether it is one process or mechanism or another, it would appear that evolutionary adaptation evolved neural circuits that may have been exploited for different uses, and one such use may be the cognitive processes engaged in memory consolidation that occur during the neurobiological states of sleep.
Therefore, the notion of neural reuse should not be limited to recycling of neural circuitry, but should extend to recycling of neurobiological processes that may have well served the evolutionary advancement in mammalian intelligence.