Procedural memory: Difference between revisions

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== Working memory ==
Models of working memory primarily focused on declarative until Oberauer suggested that declarative and procedural memory may be processed differently in working memory.<ref>{{Cite book|chapter-url=http://linkinghub.elsevier.com/retrieve/pii/S007974210951002X|last=Oberauer|first=Klaus|pages=45–100|doi=10.1016/s0079-7421(09)51002-x|title=The Psychology of Learning and Motivation|volume=51|year=2009|isbn=9780123744890|chapter=Chapter 2 Design for a Working Memory|url=https://www.zora.uzh.ch/id/eprint/28472/1/Oberauer_PLM_2009.pdf}}</ref> The working memory model is thought to be divided into two subcomponents; one is responsible for declarative, while the other represents procedural memory.<ref>{{Cite journal|last=Oberauer|first=Klaus|last2=Souza|first2=Alessandra S.|last3=Druey|first3=Michel D.|last4=Gade|first4=Miriam|title=Analogous mechanisms of selection and updating in declarative and procedural working memory: Experiments and a computational model|journal=Cognitive Psychology|volume=66|issue=2|pages=157–211|doi=10.1016/j.cogpsych.2012.11.001|pmid=23276689|year=2013|url=https://www.semanticscholar.org/paper/8e793c2e35ed77d166cd4b3f0556304e26d09f62}}</ref><ref>{{Cite journal|last=Souza|first=Alessandra da Silva|last2=Oberauer|first2=Klaus|last3=Gade|first3=Miriam|last4=Druey|first4=Michel D.|date=2012-05-01|title=Processing of representations in declarative and procedural working memory|journal=The Quarterly Journal of Experimental Psychology|volume=65|issue=5|pages=1006–1033|doi=10.1080/17470218.2011.640403|issn=1747-0218|pmid=22332900}}</ref> These two subsections are considered to be largely independent of each other.<ref>{{Cite journal|last=Gade|first=Miriam|last2=Druey|first2=Michel D.|last3=Souza|first3=Alessandra S.|last4=Oberauer|first4=Klaus|title=Interference within and between declarative and procedural representations in working memory|journal=Journal of Memory and Language|volume=76|pages=174–194|doi=10.1016/j.jml.2014.07.002|year=2014}}</ref> It has also been determined that the process for selection may be very similar in nature when considering either modality of working memory .<ref>{{Cite journal|last=Gade|first=Miriam|last2=Souza|first2=Alessandra S.|last3=Druey|first3=Michel D.|last4=Oberauer|first4=Klaus|date=2017-01-01|title=Analogous selection processes in declarative and procedural working memory: N-2 list-repetition and task-repetition costs|journal=Memory & Cognition|language=en|volume=45|issue=1|pages=26–39|doi=10.3758/s13421-016-0645-4|pmid=27517876|issn=0090-502X}}</ref>
 
==Acquisition of skill==
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===Serial reaction time task===
This task involves having participants retain and learn procedural skills that assess specific memory for procedural-motor skill.<ref>{{cite journal | last1 = Balota | first1 = D.A. | last2 = Connor | first2 = L.T. | last3 = Ferraro | first3 = F.R. | year = 1993 | title = Implicit Memory and the Formation of New Associations in Nondemented Parkinson's Disease Individuals and Individuals with Senile Dementia of the Alzheimer Type: A Serial Reaction Time (SRT) Investigation | url = https://www.semanticscholar.org/paper/9e453e33dd0980a64ef0035555e19cc28d21c304| journal = Brain and Cognition | volume = 21 | issue = 2| pages = 163–180 | doi=10.1006/brcg.1993.1013| pmid = 8442933 }}</ref> These skills are measured by observing the speed and accuracy of the participant's ability to retain and acquire new skills. The [[reaction time]] is the time it takes for the participant to respond to the designated cue presented to them.<ref name="Acquisition of Mirror Tracing">{{cite journal | last1 = Corkin | first1 = S. | last2 = Gabrieli | first2 = J. D. E. | last3 = Growdon | first3 = J. H. | last4 = Mickel | first4 = S. F. | year = 1993 | title = Intact Acquisition and Long-Term Retention of Mirror-Tracing Skill in Alzheimer's Disease and in Global Amnesia | url = https://semanticscholar.org/paper/9667d2bffca076be7a0de774dd4e92832bb77d6f| journal = Behavioral Neuroscience | volume = 107 | issue = 6| pages = 899–910 | doi=10.1037/0735-7044.107.6.899| pmid = 8136066 }}</ref> Participants with Alzheimer's disease and amnesia demonstrate a long retention time which indicates that they are able to retain the skill and demonstrate effective performance of the task at a later point in time.<ref name="Acquisition of Mirror Tracing"/>
 
===Mirror tracing task===
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=== Choice reaction task ===
Choice reaction tasks have been used to assess working memory.<ref>{{Cite journal|last=Shahar|first=Nitzan|last2=Teodorescu|first2=Andrei R.|last3=Usher|first3=Marius|last4=Pereg|first4=Maayan|last5=Meiran|first5=Nachshon|title=Selective influence of working memory load on exceptionally slow reaction times.|journal=Journal of Experimental Psychology: General|language=en|volume=143|issue=5|pages=1837–1860|doi=10.1037/a0037190|pmid=25000446|year=2014}}</ref> It has been determined to be useful in gauging procedural working memory by asking participants to follow stimulus-reaction rules.<ref name="Shahar 197–204">{{Cite journal|last=Shahar|first=Nitzan|last2=Teodorescu|first2=Andrei R.|last3=Anholt|first3=Gideon E.|last4=Karmon-Presser|first4=Anat|last5=Meiran|first5=Nachshon|title=Examining procedural working memory processing in obsessive-compulsive disorder|journal=Psychiatry Research|volume=253|pages=197–204|doi=10.1016/j.psychres.2017.03.048|pmid=28390295|year=2017|url=https://www.semanticscholar.org/paper/eeea2f4d120b48c71320a903eb0bb5c5061509eb}}</ref>
 
==Expertise==
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== Genetic influence ==
Genetic makeup has been found to impact skill learning and performance, and therefore plays a role in achieving expertise. Using the pursuit rotor task, one study examined the effects of [[Practice (learning method)|practice]] in identical and fraternal twins raised in separate homes. Because identical twins share 100% of their genes while fraternal twins share 50%, the impact of genetic makeup on skill learning could be examined. The results of the pursuit rotor task test became more identical with practice over time for the identical twins, whereas the results for the fraternal twins became more disparate with practice. In other words, the performance of the skill by the identical twins became closer to 100% identical, while the fraternal twins' skill performance became less identical, suggesting the 50% difference in genetic makeup is responsible for the difference in skill performance. The study shows that more practice leads to a closer representation of a person's innate capability, also known as [[Aptitude|talent]]. Therefore, some of the differences people show after extended practice increasingly reflects their genetics. The study also confirmed the idea that practice improves skill learning by showing that, in both the identical and fraternal groups, more practice aided in shedding ineffective tendencies in order to improve execution of a given skill.<ref>{{Cite journal|last=Fox|first=Paul W.|last2=Hershberger|first2=Scott L.|last3=Bouchard|first3=Thomas J.|date=1996-11-28|title=Genetic and environmental contributions to the acquisition of a motor skill|journal=Nature|language=en|volume=384|issue=6607|pages=356–358|doi=10.1038/384356a0|pmid=8934520|bibcode=1996Natur.384..356F|url=https://www.semanticscholar.org/paper/afa191e4026af47dbe915c19349046eba4c4c1e3}}</ref><ref>{{Cite book|title=Learning and memory : from brain to behavior|last=Eduardo.|first=Mercado|last2=E.|first2=Myers, Catherine|date=2014-01-01|publisher=Worth Publishers|isbn=9781429240147|___location=|pages=307–308|oclc=900627172}}</ref> Currently, the link between [[learning]] and genetics has been limited to simple task learning, while a link to more complex forms of learning, such as the learning of [[cognitive skill]]s, has not been confirmed.<ref>{{Cite journal|last=Wulf|first=Gabriele|last2=Shea|first2=Charles H.|date=2002-06-01|title=Principles derived from the study of simple skills do not generalize to complex skill learning|journal=Psychonomic Bulletin & Review|language=en|volume=9|issue=2|pages=185–211|doi=10.3758/BF03196276|pmid=12120783|issn=1069-9384}}</ref>
 
==Anatomical structures==
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The [[dorsolateral]] striatum is associated with the acquisition of habits and is the main neuronal cell nucleus linked to procedural memory. Connecting excitatory [[afferent nerve fiber]]s help in the regulation of activity in the basal ganglia circuit. Essentially, two parallel information processing pathways diverge from the striatum. Both acting in opposition to each other in the control of movement, they allow for association with other needed functional structures<ref>{{cite journal | last1 = Alexander | first1 = GE | last2 = Crutcher | first2 = MD | year = 1990 | title = Functional architecture of basal ganglia circuits; neural substrates of parallel processing | url = | journal = Trends Neurosci | volume = 13 | issue = 7| pages = 266–271 | doi=10.1016/0166-2236(90)90107-l | pmid=1695401}}</ref> One pathway is direct while the other is indirect and all pathways work together to allow for a functional neural feedback loop. Many looping circuits connect back at the striatum from other areas of the brain; including those from the emotion-center linked limbic cortex, the reward-center linked [[ventral striatum]] and other important motor regions related to movement.<ref>{{cite journal | last1 = Haber | first1 = SN | last2 = Fudge | first2 = JL | last3 = McFarland | first3 = NR | year = 2000 | title = Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum | url = | journal = J. Neurosci. | volume = 20 | issue = 6| pages = 2369–2382 | doi = 10.1523/JNEUROSCI.20-06-02369.2000 }}</ref> The main looping circuit involved in the motor skill part of procedural memory is usually called the cortex-basal ganglia-thalamus-cortex loop.<ref>{{cite journal | last1 = Parent | first1 = A | year = 1990 | title = Extrinsic connections of the basal ganglia | url = | journal = Trends Neurosci | volume = 13 | issue = 7| pages = 254–258 | doi=10.1016/0166-2236(90)90105-j| pmid = 1695399 }}</ref>
 
The striatum is unique because it lacks the [[glutamate]]-related neurons found throughout most of the brain. Instead, it is categorized by a high concentration of a special type of [[GABA]] related inhibiting cell known as the [[medium spiny neuron]].<ref>{{cite journal | last1 = Smith | first1 = Y. | last2 = Raju | first2 = D. V. | last3 = Pare | first3 = J. F. | last4 = Sidibe | first4 = M. | year = 2004 | title = The thalamostriatal system: a highly specific network of the basal ganglia circuitry | url = https://www.semanticscholar.org/paper/99588f5770f5388d0c260eb6b70b9c88ebff0171| journal = Trends Neurosci | volume = 27 | issue = 9| pages = 520–527 | doi=10.1016/j.tins.2004.07.004| pmid = 15331233 }}</ref> The two parallel pathways previously mentioned travel to and from the striatum and are made up of these same special medium spiny neurons. These neurons are all sensitive to different neurotransmitters and contain a variety of corresponding receptors including dopamine receptors ([[DRD1]], [[DRD2]]), [[muscarinic receptors]] (M4) and [[adenosine receptors]] (A2A). Separate interneurons are known to communicate with striatal spiny neurons in the presence of the [[somatic nervous system]] neurotransmitter [[acetylcholine]].<ref>{{cite journal | last1 = Zhou | first1 = FM | last2 = Wilson | first2 = CJ | last3 = Dani | first3 = JA | year = 2002 | title = Cholinergic Interneuron characteristics and nicotinic properties in the striatum | url = | journal = J. Neurobiol. | volume = 53 | issue = 4| pages = 590–605 | doi=10.1002/neu.10150 | pmid=12436423}}</ref>
 
Current understanding of brain anatomy and physiology suggests that striatal neural plasticity is what allows basal ganglia circuits to communicate between structures and to functionally operate in procedural memory processing.<ref>{{cite journal | last1 = Kreitzer | first1 = AC | year = 2009 | title = Physiology and pharmacology of striatal neurons | url = | journal = Annual Review of Neuroscience| volume = 32 | issue = | pages = 127–47 | doi=10.1146/annurev.neuro.051508.135422| pmid = 19400717 }}</ref>
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{{details|topic=dopamine|Dopamine}}
[[File:Dopamine Pathways.png|thumb|right|Dopamine Pathways in the brain highlighted in Blue]]
[[Dopamine]] is one of the more known neuromodulators involved in procedural memory. Evidence suggests that it may influence neural plasticity in memory systems by adapting brain processing when the environment is changing and an individual is then forced to make a behavioural choice or series of rapid decisions. It is very important in the process of "adaptive navigation", which serves to help different brain areas respond together during a new situation that has many unknown stimuli and features.<ref>{{cite journal | last1 = Mizumori | first1 = SJ | last2 = Puryear | first2 = CB | last3 = Martig | first3 = AK | date = Apr 2009 | title = Basal ganglia contributions to adaptive navigation | url = https://www.semanticscholar.org/paper/178d090cf12f5228b4db2aa08208bcfb1482b02c| journal = Behav. Brain Res. | volume = 199 | issue = 1| pages = 32–42 | doi=10.1016/j.bbr.2008.11.014| pmid = 19056429 }}</ref> Dopamine pathways are dispersed all over the brain and this allows for parallel processing in many structures all at the same time. Currently most research points to the [[Mesocortical pathway|mesocorticolimbic]] dopamine pathway as the system most related to reward learning and psychological conditioning.<ref>{{cite journal | last1 = Zellner | first1 = MR | last2 = Rinaldi | first2 = R | year = 2009 | title = How conditioned stimuli acquire the ability to activate VTA dopamine cells; A proposed neurobiological component of reward-related learning | url = https://www.semanticscholar.org/paper/e1c3bddf2fbca3ca33cdf956ac96afa5c13fe10e| journal = Neurosci. Biobehav. Rev. | volume = 34| issue = 5| pages = 769–780| doi=10.1016/j.neubiorev.2009.11.011| pmid = 19914285 }}</ref>
 
===At the synapse===
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Current Research indicates that procedural memory problems in [[Alzheimer's]] may be caused by changes in enzyme activity in memory-integrating brain regions such as the hippocampus. The specific enzyme linked to these changes is called [[acetylcholinesterase]] (AchE) which may be affected by a genetic predisposition in an immune-system brain receptor called the histamine H1 receptor. The same current scientific information also looks at how [[dopamine]], [[serotonin]] and [[acetylcholine]] neurotransmitter levels vary in the cerebellum of patients that have this disease. Modern findings advance the idea that the [[histamine]] system may be responsible for the cognitive deficits found in Alzheimer's and for the potential procedural memory problems that may develop as a result of the [[psychopathology]].<ref>{{cite journal | last1 = Dere | first1 = E. | last2 = Zlomuzica | first2 = A. | last3 = Viggiano | first3 = D. | last4 = Ruocco | first4 = L.A. | last5 = Watanabe | first5 = T. | last6 = Sadile | first6 = A.G. | last7 = Huston | first7 = J.P. | last8 = Souza-Silva | first8 = M.A. De | year = 2008 | title = Episodic-like and procedural memory impairments in histamine H1 Receptor knockout mice coincide with changes in acetylcholine esterase activity in the hippocampus and dopamine turnover in the cerebellum | url = https://www.semanticscholar.org/paper/c8b0f50f59a44c6d2308d4ae2fea7e893eb8affc| journal = Neuroscience | volume = 157 | issue = 3| pages = 532–541 | doi=10.1016/j.neuroscience.2008.09.025 | pmid=18926883}}</ref>
 
===Tourette syndrome===
{{details|topic=Tourette syndrome|Tourette syndrome}}
This disease of the central nervous system, like many other procedural-memory related disorders, involves changes in the associated subcortical brain area known as the striatum. This area and the brain circuits closely interacting with it from the basal ganglia are affected both structurally and at a more functional level in the people affected by [[Tourette's syndrome]]. Current literature on this topic provides evidence for there being many unique forms of procedural memory. The one most relevant to procedural memory and most common in Tourette's is related to the skill-acquisition process that ties stimuli to response during the learning part of procedural memory.<ref>{{cite journal | last1 = Marsh | first1 = R | last2 = Alexander | first2 = GM | last3 = Packard | first3 = MG | last4 = Zhu | first4 = H | last5 = Peterson | first5 = BS | year = 2005 | title = Perceptual-motor skill learning in Gilles de la Tourette syndrome. Evidence for multiple procedural learning and memory systems | url = https://www.semanticscholar.org/paper/0afcdec2a12b0b52bd503da17c006fd921a3c15a| journal = Neuropsychologia | volume = 43 | issue = 10| pages = 1456–65 | doi=10.1016/j.neuropsychologia.2004.12.012 | pmid=15989936}}</ref>
 
One study has found that those with Tourette syndrome have enhanced procedural learning. Subjects with Tourette's syndrome were found to have more quickly processed procedural knowledge and more accurately learned procedural skills than their typically developed counterparts. Another study found that subjects with Tourette's syndrome displayed faster processing of rule-based grammar than typically developed subjects. Two possible explanations exist for these results. One explanation is that once a person with Tourette's syndrome has learned a procedure, there is a mechanism that supports more accelerated processing. Second, because procedural memory subserves sequencing, and grammar recruits sequencing, an enhancement of grammatical processing was seen in those with Tourette's syndrome due to their improved procedural memories.<ref>{{cite journal | last1 = Takács | first1 = A | last2 = et | first2 = al. | title = Is procedural memory enhanced in Tourette syndrome? Evidence from a sequence learning task | journal = Cortex | volume = 100 | pages = 84–94 | year = 2017 | doi=10.1016/j.cortex.2017.08.037| pmid = 28964503 | url = http://eprints.gla.ac.uk/149676/7/149676.pdf }}</ref>
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===Human immunodeficiency virus (HIV)===
{{details|topic=human immunodeficiency virus|HIV}}
Neural systems used by procedural memory are commonly targeted by [[Human Immunodeficiency Virus]]; the striatum being the structure most notably affected.<ref>{{cite journal | last1 = Reger | first1 = M | last2 = Welsh | first2 = R | last3 = Razani | first3 = J | last4 = Martin | first4 = DJ | last5 = Boone | first5 = KB | year = 2002 | title = A meta-analysis of the neuropsychological sequelae of HIV infection | url = | journal = Journal of the International Neuropsychological Society | volume = 8 | issue = 3| pages = 410–424 | doi=10.1017/s1355617702813212| pmid = 11939699 }}</ref> MRI studies have even shown white matter irregularity and basal ganglia subcortical atrophy in these vital areas necessary for both procedural memory and motor-skill.<ref>{{cite journal | last1 = Chang | first1 = L | last2 = Lee | first2 = PL | last3 = Yiannoutsos | first3 = CT | last4 = Ernst | first4 = T | last5 = Marra | first5 = CM | last6 = Richards | first6 = T | display-authors = etal | year = 2004 | title = A multicenter in vivo proton-MRS study of HIV-associated dementia and its relationship to age | url = https://www.semanticscholar.org/paper/f773811cd3929a13639cb15fa8cedcf5f0e01212| journal = NeuroImage | volume = 23 | issue = 4| pages = 1336–1347 | doi=10.1016/j.neuroimage.2004.07.067 | pmid=15589098}}</ref> Applied research using various procedural memory tasks such as the Rotary pursuit, Mirror star tracing and Weather prediction tasks have shown that HIV positive individuals perform worse than HIV negative participants suggesting that poorer overall performance on tasks is due to the specific changes in the brain caused by the disease.<ref>{{cite journal | last1 = Gonzalez | first1 = R | last2 = Jacobus | first2 = J | last3 = Amatya | first3 = AK | last4 = Quartana | first4 = PJ | last5 = Vassileva | first5 = J | last6 = Martin | first6 = EM | year = 2008 | title = Deficits in complex motor functions, despite no evidence of procedural learning deficits, among HIV+ individuals with history of substance dependence | url = | journal = Neuropsychology | volume = 22 | issue = 6| pages = 776–86 | doi=10.1037/a0013404| pmid = 18999351 | pmc = 2630709 }}</ref>
 
===Huntington's disease===
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===Schizophrenia===
{{details|topic=schizophrenia|Schizophrenia}}
MRI studies have shown that [[schizophrenic]] patients not currently taking related medication have a smaller putamen; part of the striatum that plays a very important role in procedural memory.<ref>{{cite journal | last1 = Lang | first1 = DJ | last2 = Kopala | last3 = Smith | first3 = GN | display-authors = etal | year = 1999 | title = MRI study of basal ganglia volumes in drug-naive first-episode patients with schizophrenia | url = | journal = Schizophr Res | volume = 36 | issue = | page = 202 }}</ref> Further studies on the brain reveal that schizophrenics have improper basal ganglia communication with the surrounding extrapyramidal system that is known to be closely involved with the motor system and in the coordination of movement.<ref>A Chatterjee, M Chakos, A Koreen, S Geisler, B Sheitman, M Woerner, JM Kane J Alvir and Ja (1995). "Prevalence and clinical correlates of extrapyramidal signs and spontaneous dyskinesia in never-medicated schizophrenic patients" ''Am J Psychiatry'' 1995 Dec; 152 (12); 1724-9.</ref> The most recent belief is that functional problems in the striatum of schizophrenic patients are not significant enough to seriously impair procedural learning, however, research shows that the impairment will be significant enough to cause problems improving performance on a task between practice intervals.<ref>{{cite journal | last1 = Schérer | first1 = H | last2 = Stip | first2 = E | last3 = Paquet | first3 = F | last4 = Bédard | first4 = MA | date = Winter 2003 | title = Mild procedural learning disturbances in neuroleptic-naive patients with schizophrenia | url = | journal = J NeuropsychiatryJournal Clin Neurosciof Neuropsychiatry| volume = 15 | issue = 1| pages = 58–63 | doi=10.1176/appi.neuropsych.15.1.58| pmid = 12556572 }}</ref>
 
==Drugs==
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===Cocaine===
{{details|topic=cocaine|Cocaine}}
It is evident that long-term [[Cocaine]] abuse alters brain structures. Research has shown that the brain structures that are immediately affected by long-term cocaine abuse include: cerebral [[hypoperfusion]] in the frontal, periventricular and temporal-parietal.<ref name="cocaine abuse">{{cite journal | last1 = Strickland | first1 = T. L. | last2 = Mena | first2 = I. | last3 = Villanueva-Meyer | first3 = J. | last4 = Miller | first4 = B. L. | last5 = Cummings | first5 = J. | last6 = Mehringer | first6 = C. M. | last7 = Satz | first7 = P. | last8 = Myers | first8 = H. | year = 1993 | title = Cerebral perfusion and neuropsychological consequences of chronic cocaine use | url = | journal = American NeuropsychiatricThe AssociationJournal of Neuropsychiatry and Clinical Neurosciences| volume = 5 | issue = 4| pages = 419–427 | doi=10.1176/jnp.5.4.419| pmid = 8286941 }}</ref> These structures play a role in various memory systems. Furthermore, the drug cocaine elicits its desirable effects by blocking the DRD1 dopamine receptors in the striatum, resulting in increased dopamine levels in the brain.<ref name="cocaine abuse"/> These receptors are important for the consolidation of procedural memory. These increased dopamine levels in the brain resultant of cocaine use is similar to the increased dopamine levels in the brain found in schizophrenics.<ref>{{cite journal | last1 = Serper | first1 = M. R. | last2 = Bermanc | first2 = A. | last3 = Copersinoa | first3 = M. L. | last4 = Choub | first4 = J. C. Y. | last5 = Richarmea | first5 = D. | last6 = Cancrob | first6 = R. | year = 2000 | title = Learning and memory impairment in cocaine-dependent and comorbid schizophrenic patients | url = | journal = Psychiatry Research | volume = 93 | issue = 1| pages = 21–32 | doi=10.1016/s0165-1781(99)00122-5| pmid = 10699225 }}</ref> Studies have compared the common memory deficits caused by both cases to further understand the neural networks of procedural memory. To learn more about the effects of dopamine and its role in schizophrenia see: [[dopamine hypothesis of schizophrenia]]. Studies using rats have shown that when rats are administered trace amounts of cocaine, their procedural memory systems are negatively impacted. Specifically, the rats are unable to effectively consolidate motor-skill learning.<ref>Willuhn I, Steiner H. (2008) Motor-skill learning in a novel running-wheel task is dependent on D1 dopamine receptors in the striatum. ''Neuroscience'', 22 April; 153 (1); 249-58. Epub 2008 Feb 6.</ref> With cocaine abuse being associated with poor procedural learning, research has shown that abstinence from cocaine is associated with sustained improvement of motor-skill learning (Wilfred et al.).
 
===Psychostimulants===
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==Sleep==
Practice is clearly an important process for learning and perfecting a new skill. With over 40 years of research, it is well established in both humans and animals that the formation of all forms of memory are greatly enhanced during the brain-state of sleep. Furthermore, with humans, sleep has been consistently shown to aid in the development of procedural knowledge by the ongoing process of memory consolidation, especially when sleep soon follows the initial phase of memory acquisition.<ref>{{cite journal | last1 = Karni | first1 = A. | last2 = Tanne | first2 = D. | last3 = Rubenstein | first3 = B.S. | last4 = Askenasy | first4 = J.J. | last5 = Sagi | first5 = D. | year = 1994 | title = Dependence on REM sleep of overnight improvement of a perceptual skill | url = | journal = Science | volume = 265 | issue = 5172| pages = 679–682 | doi=10.1126/science.8036518| pmid = 8036518 | bibcode = 1994Sci...265..679K }}</ref><ref>{{cite journal | last1 = Gais | first1 = S. | last2 = Plihal | first2 = W. | last3 = Wagner | first3 = U. | last4 = Born | first4 = J. | year = 2000 | title = Early sleep triggers memory for early visual discrimination skills | url = https://www.semanticscholar.org/paper/ba7d00d764e18b32c63b0eae5a5edf9854b09c28| journal = Nat. Neurosci. | volume = 3 | issue = 12| pages = 1335–1339 | doi=10.1038/81881| pmid = 11100156 }}</ref><ref>{{cite journal | last1 = Stickgold | first1 = R. | last2 = James | first2 = L. | last3 = Hobson | first3 = J.A. | year = 2000a | title = Visual discrimination learning requires sleep after training | url = | journal = Nat. Neurosci. | volume = 3 | issue = 12| pages = 1237–1238 | doi=10.1038/81756| pmid = 11100141 }}</ref><ref>{{cite journal | last1 = Stickgold | first1 = R. | last2 = Whidbee | first2 = D. | last3 = Schirmer | first3 = B. | last4 = Patel | first4 = V. | last5 = Hobson | first5 = J.A. | year = 2000b | title = Visual discrimination task improvement: A multi-step process occurring during sleep | url = https://www.semanticscholar.org/paper/f635eb5e63eff7dc17c1b0b9548f80b1b35b76cf| journal = J. Cogn. Neurosci. | volume = 12 | issue = 2| pages = 246–254 | doi=10.1162/089892900562075| pmid = 10771409 }}</ref><ref>{{cite journal | last1 = Walker | first1 = M.P. | last2 = Brakefield | first2 = T. | last3 = Morgan | first3 = A. | last4 = Hobson | first4 = J.A. | last5 = Stickgold | first5 = R. | year = 2002 | title = Practice with sleep makes perfect: Sleep dependent motor skill learning | url = | journal = Neuron | volume = 35 | issue = 1| pages = 205–211 | doi=10.1016/s0896-6273(02)00746-8 | pmid=12123620}}</ref> Memory consolidation is a process that transforms novel memories from a relatively fragile state to a more robust and stable condition. For a long time it was believed that the consolidation of procedural memories took place solely as a function of time,<ref>{{cite journal | last1 = Brashers-Krug | first1 = T. | last2 = Shadmehr | first2 = R. | last3 = Bizzi | first3 = E. | year = 1996 | title = Consolidation in human motor memory | url = | journal = Nature | volume = 382 | issue = 6588| pages = 252–255 | doi=10.1038/382252a0| pmid = 8717039 | citeseerx = 10.1.1.39.3383 | bibcode = 1996Natur.382..252B }}</ref><ref>{{cite journal | last1 = McGaugh | first1 = J.L. | year = 2000 | title = Memory—A century of consolidation | url = https://semanticscholar.org/paper/4599cc62e637a5619b3f9ee8dd2326d7288cbb1c| journal = Science | volume = 287 | issue = 5451| pages = 248–251 | doi=10.1126/science.287.5451.248 | pmid=10634773| bibcode = 2000Sci...287..248M }}</ref> but more recent studies suggest, that for certain forms of learning, the consolidation process is exclusively enhanced during periods of sleep.<ref>{{cite journal | last1 = Fischer | first1 = S. | last2 = Hallschmid | first2 = M. | last3 = Elsner | first3 = A.L. | last4 = Born | first4 = J. | year = 2002 | title = Sleep forms memory for finger skills | url = | journal = Proc. Natl. Acad. Sci. USA | volume = 99 | issue = 18| pages = 11987–11991 | doi=10.1073/pnas.182178199| pmid = 12193650 | pmc = 129381 | bibcode = 2002PNAS...9911987F }}</ref> However, it is important to note that not just any type of sleep is sufficient to improve procedural memory and performance on subsequent procedural tasks. In fact, within the ___domain of motor skill, there is evidence showing that no improvement on tasks is shown following a short, [[non-rapid eye movement]] (NREM; stages 2–4) sleep, such as a nap.<ref>{{cite journal | last1 = Siegel | first1 = J. M. | year = 2001 | title = The REM sleep-memory consolidation hypothesis | url = | journal = Science | volume = 294 | issue = 5544| pages = 1058–1063 | doi=10.1126/science.1063049| pmid = 11691984 | bibcode = 2001Sci...294.1058S }}</ref> [[REM sleep]] following a period of [[slow-wave sleep]] (SWS; combined stage 3 and 4 and the deepest form of NREM sleep), has shown to be the most beneficial type of sleep for procedural memory enhancement, especially when it takes place immediately after the initial acquisition of a skill. So essentially, a full night (or day) of uninterrupted sleep soon after learning a skill will allow for the most memory consolidation possible. Furthermore, if REM sleep is disrupted, there is no gain in procedural performance shown.<ref>{{cite journal | last1 = Karni | first1 = A. | last2 = Meyer | first2 = G. | last3 = Rey-Hipolito | first3 = C. | last4 = Jezzard | first4 = P. | last5 = Adams | first5 = M.M. | last6 = Turner | first6 = R. | last7 = Ungerleider | first7 = L.G. | year = 1998 | title = The acquisition of skilled motor performance: Fast and slow experience-driven changes in primarymotor cortex | url = | journal = Proc. Natl. Acad. Sci. USA | volume = 95 | issue = 3| pages = 861–868 | doi=10.1073/pnas.95.3.861| pmid = 9448252 | pmc = 33809 | bibcode = 1998PNAS...95..861K }}</ref> However, equal improvement will take place whether the sleep after practice was at night or during the daytime, as long as SWS is followed by REM sleep. It has also been shown that the enhancement in memory is specific to the learned stimulus (i.e., learning a running technique will not cross over to improvements in biking performance).<ref>{{cite journal | last1 = Mednick | first1 = S.C. | display-authors = etal | year = 2003 | title = Sleep-dependent learning: a nap is as good as a night | url = https://www.semanticscholar.org/paper/ee698a6866fc21686c4e6798f0c3dbc13e568d2d| journal = Nat. Neurosci. | volume = 6 | issue = 7| pages = 697–698 | doi=10.1038/nn1078 | pmid=12819785}}</ref> Subject performance in the Wff 'n Proof Task,<ref>Smith C. REM sleep and learning: some recent findings. In: Moffit A, Kramer M, Hoffman H, editors. The functions of dreaming. Albany:SUNY; 1993.</ref><ref>{{cite journal | last1 = Smith | first1 = C | last2 = Fazekas | first2 = A | year = 1997 | title = Amount of REM sleep and Stage 2 sleep required for efficient learning | url = | journal = Sleep Res | volume = 26 | issue = | page = 690 }}</ref><ref>{{cite journal | last1 = Smith | first1 = C | last2 = Weeden | first2 = K | year = 1990 | title = Post training REMs coincident auditory stimulation enhances memory in humans | url = | journal = Psychiatr J Univ Ott | volume = 15 | issue = 2| pages = 85–90 | pmid = 2374793 }}</ref> the [[Tower of Hanoi]],<ref>{{cite journal | last1 = Smith | first1 = CT | last2 = Nixon | first2 = MR | last3 = Nader | first3 = RS | year = 2004 | title = Post training increases in REM sleep intensity implicate REM sleep in memory processing and provide a biological marker of learning potential | url = | journal = Learn Mem | volume = 11 | issue = 6| pages = 714–9 | doi=10.1101/lm.74904| pmid = 15576889 | pmc = 534700 }}</ref> and the Mirror Tracing Task<ref>Conway J, Smith C. REM sleep and learning in humans: a sensitivity to specific types of learning tasks. In: Proceedings of the 12th Congress of the European Sleep Research Society. 1994.</ref> has been found to improve following REM sleep periods.
 
Whether a skill is learned explicitly (with [[attention]]) or implicitly, each plays a role in the offline consolidation effect. Research suggests that explicit awareness and understanding of the skill being learned during the acquisition process greatly improves the consolidation of procedural memories during sleep.<ref>{{cite journal | last1 = Robertson | first1 = E.M. | display-authors = etal | year = 2004 | title = Awareness modifies skill-learning benefits of sleep | url = | journal = Curr. Biol. | volume = 14 | issue = 3| pages = 208–212 | doi=10.1016/s0960-9822(04)00039-9}}</ref> This finding is not surprising, as it is widely accepted that intention and awareness at time of learning enhances the acquisition of most forms of memory.