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  • Print publication year: 2011
  • Online publication date: November 2011

14 - The medial reticular formation: a brainstem substrate for simple action selection?

from Part II - Computational neuroscience models



The search for the neural substrate of vertebrate action selection has focused on structures in the fore- and mid-brain, particularly on the basal ganglia. Yet, the behavioural repertoire of decerebrate and neonatal animals suggests the existence of a relatively self-contained neural substrate for action selection in the brainstem. We propose that the medial reticular formation (mRF) is this substrate's main component, reviewing evidence that the mRF's inputs, outputs, and intrinsic organisation are consistent with the requirements of an action selection system. We argue that the internal architecture of the mRF is composed of interconnected neuron clusters; our quantitative model of this anatomy suggests the mRF's intrinsic circuitry constitutes a small-world network, and may have evolved to reduce axonal wiring. We use computational models to enumerate and illustrate potential configurations of action representation within the internal circuitry of the mRF. We show that each cluster's output could represent activation of an action component; thus, co-activation of a set of these clusters would lead to the coordinated behavioural response observed in the animal. New results are presented that provide evidence for an alternative scheme: inputs to the mRF are organised to contact clusters, but recruit a pattern of reticulo-spinal neurons from across clusters to generate an action. We propose that this reconciles the anatomical structure with behavioural data showing action sequencing is degraded, rather than individual actions lost, as the mRF is progressively lesioned. Finally, we consider the potential integration of the basal ganglia and mRF substrates for selection and suggest they may collectively form a layered/hierarchical control system.


All animals must continuously sequence and coordinate behaviours appropriate to both their context and current internal state if they are to survive. It is natural to wonder what parts of the nervous system – the neural substrate – evolved to carry out this action selection process. For simpler animals, like the nematode worm Caenorhabditis elegans and the leech, a circumscribed behavioural repertoire is handled by specialist neurons that direct motor responses to specific stimuli (de Bono and Maricq, 2005; Kristan et al., 2005; Stephens et al., 2008). The sensory apparatus and motor behaviours are largely a product of these animals’ ecological niche, and hence so too is the neural network that handles the action selection process.

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Albert., RBarabasi, A.-L 2002 Statistical mechanics of complex networksRev. Mod. Phys 74 47
Alford, S.Zompa, I.Dubuc, R. 1995 Long-term potentiation of glutamatergic pathways in the lamprey brainstemJ Neurosci 15 7528
Angel, A. 1977 Processing of sensory informationProg. Neurobiol. 9 1
Berntson, G. G.Micco, D. J. 1976 Organization of brainstem behavioral systemsBrain Res. Bull. 1 471
Berridge, K. C. 1989 Progressive degradation of serial grooming chains by descending decerebrationBehav. Brain Res. 33 241
Berridge, K. C.Whishaw, I. Q. 1992 Cortex, striatum and cerebellum: control of serial order in a grooming sequenceExp. Brain Res. 90 275
Blessing, W. W. 1997 The Lower Brainstem and Bodily HomeostasisNew YorkOxford University Press
Bowsher, D. 1970 Place and modality analysis in caudal reticular formationJ. Physiol. 209 473
Bowsher, D.Westman, J. 1971 Ultrastructural characteristics of the caudal and rostral brain stem reticular formationBrain Res 28 443
Braak, H.Rub, U.Sandmann-Keil, D. 2000 Parkinson's disease: affection of brain stem nuclei controlling premotor and motor neurons of the somatomotor systemActa Neuropathol. (Berl.) 99 489
Braitenberg, V. 1984 Vehicles: Experiments in Synthetic PsychologyCambridge, MAMIT Press
Breedlove, S. M.McGinty, D. J.Siegel, J. M. 1979 Operant conditioning of pontine gigantocellular unitsBrain Res. Bull 4 663
Bretzner, F.Brownstone, R. M. 2008 Characterization of genetically identified reticulospinal pathways2008 Neuroscience Meeting PlannerWashington, DCSociety for Neuroscience,
Brooks, R. A. 1991 New approaches to roboticsScience 253 1227
Cant, N. B.Benson, C. G. 2003 Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nucleiBrain Res. Bull. 60 457
Cherniak, C. 1994 Component placement optimization in the brainJ. Neurosci. 14 2418
Bono, M.Maricq, A. V. 2005 Neuronal substrates of complex behaviors in C. elegansAnnu. Rev. Neurosci 28 451
Deliagina, T. G.Zelenin, P. V.Fagerstedt, P.Grillner, S.Orlovsky, G. N. 2000 Activity of reticulospinal neurons during locomotion in the freely behaving lampreyJ. Neurophysiol 83 853
Deliagina, T. G.Zelenin, P. V.Orlovsky, G. N. 2002 Encoding and decoding of reticulospinal commandsBrain Res. Rev 40 166
Delwaide, P. J.Pepin, J. L.De Pasqua, Noordhout, A. M. 2000 Projections from basal ganglia to tegmentum: a subcortical route for explaining the pathophysiology of Parkinson's disease signsJ. Neurol. 247 75
Doya, K. 1999 What are the computations of the cerebellum, the basal ganglia and the cerebral cortexNeural Networks 12 961
Drew, T.Rossignol, S. 1990 Functional organization within the medullary reticular formation of intact unanesthetized cat. I. Movements evoked by microstimulationJ. Neurophysiol. 64 767
Dubuc, R.Brocard, F.Antri, M. 2008 Initiation of locomotion in lampreysBrain Res. Rev 57 172
Eccles, J. C.Nicoll, R. A.Rantucci, T.Taborikova, H.Willey, T. J. 1976 Topographic studies on medial reticular nucleusJ. Neurophysiol. 39 109
Fay, R.Kubin, L. 2000 Pontomedullary distribution of 5-HT2A receptor-like protein in the ratJ. Comp. Neurol 418 323
Fields, H. L.Basbaum, A. I. 1978 Brainstem control of spinal pain-transmission neuronsAnnu. Rev. Physiol. 40 217
Graybiel, A. M. 1995 Building action repertoires: memory and learning functions of the basal gangliaCurr. Opin. Neurobiol. 5 733
Grillner, S.Deliagina, T.Ekeberg, O. 1995 Neural networks that co-ordinate locomotion and body orientation in lampreyTrends Neurosci 18 270
Grillner, S.Hellgren, J.Menard, A.Saitoh, K.Wikstrom, M. A. 2005 Mechanisms for selection of basic motor programs – roles for the striatum and pallidumTrends Neurosci 28 364
Groves, P. M.Miller, S. W.Parker, M. V.Rebec, G. V. 1973 Organization by sensory modality in the reticular formation of the ratBrain Res. 54 207
Gurney, K.Prescott, T. J.Redgrave, P. 2001 A computational model of action selection in the basal ganglia I: a new functional anatomyBiol. Cybern. 85 401
Gurney, K.Prescott, T. J.Redgrave, P. 2001 A computational model of action selection in the basal ganglia II: analysis and simulation of behaviourBiol. Cybern. 85 411
Hammer, R. P.J.Lindsay, R. D.Scheibel, A. B. 1981 Development of the brain stem reticular core: an assessment of dendritic state and configuration in the perinatal ratDev. Brain Res 1 179
Hattox, A.Li, Y.Keller, A. 2003 Serotonin regulates rhythmic whiskingNeuron 39 343
Hobson, J. A.Scheibel, A. B. 1980 The brainstem core: sensorimotor integration and behavioral state controlNeurosci. Res. Program. Bull. 18 1
Holmes, C. J.Mainville, L. S.Jones, B. E. 1994 Distribution of cholinergic, GABAergic and serotonergic neurons in the medial medullary reticular formation and their projections studied by cytotoxic lesions in the catNeuroscience 62 1155
Holstege, G. 1995 The basic, somatic, and emotional components of the motor system in mammalsThe Rat Nervous SystemNew YorkAcademic Press137
Humphries, M. D.Gurney, K.Prescott, T. J. 2005 Is there an integrative center in the vertebrate brainstem? A robotic evaluation of a model of the reticular formation viewed as an action selection deviceAdapt. Behav. 13 97
Humphries, M. D.Gurney, K.Prescott, T. J. 2006 The brainstem reticular formation is a small-world, not scale-free, networkProc. Roy. Soc. B. 273 503
Humphries, M. D.Gurney, K.Prescott, T. J. 2007 Is there a brainstem substrate for action selectionPhil. Trans. Roy. Soc. B 362 1627
Humphries, M. D.Prescott, T. J. 2006 Distributed action selection by a brainstem neural substrate: an embodied evaluationFrom Animals to Animats 9: Proceedings of the Ninth International Conference on Simulation of Adaptive BehaviourBerlin, GermanySpringer Verlag199
Humphries, M. D.Stewart, R. D.Gurney, K. N. 2006 A physiologically plausible model of action selection and oscillatory activity in the basal gangliaJ. Neurosci 26 12921
Inglis, W. L.Winn, P. 1995 The pedunculopontine tegmental nucleus: where the striatum meets the reticular formationProg. Neurobiol. 47 1
Iwakiri, H.Oka, T.Takakusaki, K.Mori, S. 1995 Stimulus effects of the medial pontine reticular formation and the mesencephalic locomotor region upon medullary reticulospinal neurons in acute decerebrate catsNeurosci. Res. 23 47
Iwaniuk, A. N.Whishaw, I. Q. 2000 On the origin of skilled forelimb movementsTrends Neurosci. 23 372
Jones, B. E. 1990 Immunohistochemical study of choline acetyltransferase-immunoreactive processes and cells innervating the pontomedullary reticular formation in the ratJ. Comp. Neurol 295 485
Jones, B. E. 1995 Reticular formation: cytoarchitecture, transmitters, and projectionsThe Rat Nervous SystemPaxinos, G.New YorkAcademic Press155
Jones, B. E.Holmes, C. JRodriguez-Veiga, E.Mainville, L. 1991 GABA-synthesizing neurons in the medulla: their relationship to serotonin-containing and spinally projecting neurons in the ratJ. Comp. Neurol. 313 349
Jordan, L. M.Liu, J.Hedlund, P. B.Akay, T.Pearson, K. G. 2008 Descending command systems for the initiation of locomotion in mammalsBrain Res. Rev 57 183
Jung, R.Kiemel, T.Cohen, A. H. 1996 Dynamic behavior of a neural network model of locomotor control in the lampreyJ. Neurophysiol 75 1074
Kilmer, W. L.McCulloch, W. S.Blum, J. 1969 A model of the vertebrate central command systemInt. J. Man. Mach. Stud. 1 279
Kinjo, N.Atsuta, Y.Webber, M. 1990 Medioventral medulla-induced locomotionBrain Res. Bull. 24 509
Kleinfeld, D.Berg, R. W.O’Connor, S. M. 1999 Anatomical loops and their electrical dynamics in relation to whisking by ratSomatosens. Mot. Res. 16 69
Krichmar, J. L. 2008 The neuromodulatory system: a framework for survival and adaptive behavior in a challenging worldAdapt. Behav. 16 385
Kristan, W. B.Calabrese, R. L.Friesen, W. O. 2005 Neuronal control of leech behaviorProg. Neurobiol 76 279
Kropotov, J. D.Etlinger, S. C. 1999 Selection of actions in the basal ganglia thalamocortical circuits: review and modelInt. J. Psychophysiol. 31 197
Kuypers, H. G. 1964 The descending pathways to the spinal cord, their anatomy and functionProg. Brain Res. 11 178
Lakke, J. P. 1985 Axial apraxia in Parkinson's diseaseJ. Neurol. Sci. 69 37
Langhorst, P.Schulz, B.Schulz, G.Lambertz, M. 1983 Reticular formation of the lower brainstem. A common system for cardiorespiratory and somatomotor functions: discharge patterns of neighboring neurons influenced by cardiovascular and respiratory afferentsJ. Auton. Nerv. Syst. 9 411
Langhorst, P.Schulz, B. G.Seller, H.Koepchen, H. P. 1996 Convergence of visceral and somatic afferents on single neurones in the reticular formation of the lower brain stem in dogsJ. Auton. Nerv. Syst. 57 149
Laughlin, S. B.Sejnowski, T. J. 2003 Communication in neuronal networksScience 301 1870
Lovick, T. A. 1972 The behavioural repertoire of precollicular decerebrate ratsJ. Physiol. 226 4P
Lund, J. P.Kolta, A.Westberg, K. G.Scott, G. 1998 Brainstem mechanisms underlying feeding behaviorsCurr. Opin. Neurobiol. 8 718
Magoun, H. W.Rhines, R. 1946 An inhibitory mechanism in the bulbar reticular formationJ. Neurophysiol. 9 165
Marsden, C. D.Obeso, J. A. 1994 The functions of the basal ganglia and the paradox of stereotaxic surgery in Parkinson's diseaseBrain 117 877
Martin, E. M.Pavlides, C.Pfaff, D. W. 2007 Neurons in the medullary reticular formation with multimodal sensory response capacities2007 Neuroscience Meeting PlannerSan Diego, CASociety for Neuroscience
Mathias, N.Gopal, V. 2001 Small worlds: how and whyPhys. Rev. E 63
Matsuyama, K.Mori, F.Nakajima, K. 2004 Locomotor role of the corticoreticular-reticulospinal-spinal interneuronal systemProg. Brain Res. 143 239
Mesce, K.Esch, T.Kristan, W. 2008 Cellular substrates of action selection: a cluster of higher-order descending neurons shapes body posture and locomotionJ. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol 194 469
Mink, J. W.Thach, W. T. 1993 Basal ganglia intrinsic circuits and their role in behaviorCurr. Opin. Neurobiol. 3 950
Mori, S. 1987 Integration of posture and locomotion in acute decerebrate cats and in awake, freely moving catsProg. Neurobiol. 28 161
Moruzzi, G.Magoun, H. W. 1949 Brain stem reticular formation and activation of the EEGElectroenceph. Clin. Neurophysiol. 1 455
Moschovakis, A. K.Scudder, C. A.Highstein, S. M. 1996 The microscopic anatomy and physiology of the mammalian saccadic systemProg. Neurobiol. 50 133
Newman, D. B. 1985 Distinguishing rat brainstem reticulospinal nuclei by their neuronal morphology. I. Medullary nucleiJ. fur Hirnforschung 26 187
Newman, D. B. 1995 Anatomy and neurotransmitters of brainstem motor systemsAdv. Neurol. 67 219
Noga, B. R.Kriellaars, D. J.Brownstone, R. M.Jordan, L. M. 2003 Mechanism for activation of locomotor centers in the spinal cord by stimulation of the mesencephalic locomotor regionJ. Neurophysiol. 90 1464
Parvizi, J.Damasio, A. R. 2003 Neuroanatomical correlates of brainstem comaBrain 126 1524
Paxinos, G.Watson, C. 1998 The Rat Brain in Stereotaxic CoordinatesSan Diego, CAAcademic Press
Peterson, B. W. 1979 Reticulospinal projections to spinal motor nucleiAnnu. Rev. Physiol. 41 127
Prescott, T. J. 2007 Forced moves or good tricks in design space? landmarks in the evolution of neural mechanisms for action selectionAdapt. Behav 15 9
Prescott, T. J.Redgrave, P.Gurney, K. 1999 Layered control architectures in robots and vertebratesAdapt. Behav 7 99
Prisco, G. V. D.Pearlstein, E.Ray, D. L.Robitaille, R.Dubuc, R. 2000 A cellular mechanism for the transformation of a sensory input into a motor commandJ. Neurosci 20 8169
Ramon-Moliner, E.Nauta, W. J. 1966 The isodendritic core of the brain stemJ. Comp. Neurol 126 311
Redgrave, P.Prescott, T. J.Gurney, K. 1999 The basal ganglia: a vertebrate solution to the selection problemNeuroscience 89 1009
Reiner, A.Medina, L.Veenman, C. L. 1998 Structural and functional evolution of the basal ganglia in vertebratesBrain Res. Rev. 28 235
Rubchinsky, L. L.Kopell, N.Sigvardt, K. A. 2003 Modeling facilitation and inhibition of competing motor programs in basal ganglia subthalamic nucleus-pallidal circuitsProc. Natl. Acad. Sci. USA 100 14427
Salibi, N. A.Saade, N. E.Banna, N. R.Jabbur, S. J. 1980 Dorsal column input into the reticular formationNature 288 481
Scheibel, A. B. 1984 The brainstem reticular core and sensory functionHandbook of Physiology. Section 1: The Nervous SystemBethesda, MDAmerican Physiological Society213
Scheibel, M. E.Scheibel, A. B. 1958 Structural substrates for integrative patterns in the brain stem reticular coreReticular Formation of the BrainBoston, MALittle and Brown
Scheibel, M. E.Scheibel, A. B. 1967 Anatomical basis of attention mechanisms in vertebrate brainsThe Neurosciences, A Study ProgramNew YorkThe Rockefeller University Press,577
Schulz, B.Lambertz, M.Schulz, G.Langhorst, P. 1983 Reticular formation of the lower brainstem. A common system for cardiorespiratory and somatomotor functions: discharge patterns of neighboring neurons influenced by somatosensory afferentsJ. Auton. Nerv. Syst. 9 433
Schulz, G.Lambertz, M.Schulz, B.Langhorst, P.Krienke, B. 1985 Reticular formation of the lower brainstem. A common system for cardio-respiratory and somatomotor functions. Cross-correlation analysis of discharge patterns of neighbouring neuronesJ. Auton. Nerv. Syst. 12 35
Segundo, J. P.Takenaka, T.Encabo, H. 1967 Somatic sensory properties of bulbar reticular neuronsJ. Neurophysiol 30 1221
Shammah-Lagnado, S. J.Costa, M. S.Ricardo, J. A. 1992 Afferent connections of the parvocellular reticular formation: a horseradish peroxidase study in the ratNeuroscience 50 403
Siegel, J. M. 1979 Behavioral functions of the reticular formationBrain Res. Rev. 1 69
Siegel, J. M.Nienhuis, R.Wheeler, R. L.McGinty, D. J.Harper, R. M. 1981 Discharge pattern of reticular-formation unit pairs in waking and REM-sleepExp. Neurol. 74 875
Siegel, J. M.Tomaszewski, K. S. 1983 Behavioral organization of reticular formation: studies in the unrestrained cat. I. Cells related to axial, limb, eye, and other movementsJ. Neurophysiol. 50 696
Sperry, R. W. 1952 Neurology and the mind-brain problemAmer. Sci. 40 291
Sprague, J. M.Chambers, W. W. 1954 Control of posture by reticular formation and cerebellum in the intact, anesthetized and unanesthetized, decerebrated catAm. J. Physiol. 176 52
Stephens, G. J.Johnson-Kerner, B.Bialek, W.Ryu, W. S. 2008 Dimensionality and dynamics in the behavior of C. elegansPLoS Comput. Biol 4
Stevens, D. R.Birnstiel, S.Gerber, U.McCarley, R. W.Greene, R. W. 1993 Nicotinic depolarizations of rat medial pontine reticular formation neurons studied in vitroNeuroscience 57 419
Stevens, D. R.McCarley, R. W.Greene, R. W. 1992 Serotonin1 and serotonin2 receptors hyperpolarize and depolarize separate populations of medial pontine reticular formation neurons in vitroNeuroscience 47 545
Stevens, D. R.McCarley, R. W.Greene, R. W. 1994 The mechanism of noradrenergic alpha 1 excitatory modulation of pontine reticular formation neuronsJ. Neurosci 14 6481
Swanson, L. W. 2000 Cerebral hemisphere regulation of motivated behaviorBrain Res 886 113
Szokol, K.Glover, J. C.Perreault, M.-C. 2008 Differential origin of reticulospinal drive to motorneurons innervating trunk and hindlimb muscles in the mouse revealed by optical recordingJ. Physiol 586 5259
Takakusaki, K.Saitoh, K.Harada, H.Kashiwayanagi, M. 2004 Role of basal ganglia-brainstem pathways in the control of motor behaviorsNeurosci. Res. 50 137
Torvik, A.Brodal, A. 1957 The origin of reticulospinal fibers in the cat; an experimental studyAnat. Rec. 128 113
Valverde, F. 1961 Reticular formation of the pons and medulla oblongata: a Golgi studyJ. Comp. Neurol 116 71
Whelan, P. J. 1996 Control of locomotion in the decerebrate catProg. Neurobiol. 49 481
Woods, J. W. 1964 Behavior of chronic decerebrate ratsJ. Neurophysiol. 27 635
Yates, B. J.Stocker, S. D. 1998 Integration of somatic and visceral inputs by the brainstem: functional considerationsExp. Brain Res. 119 269
Yen, J. C.Chan, S. H. 1993 Passive biophysical membrane properties of nucleus reticularis gigantocellularis neurons in brain slices from the ratNeurosci. Lett. 159 5
Zahm, D. S. 2006 The evolving theory of basal forebrain functional–anatomical ‘macrosystems’Neurosci. Biobehav. Rev 30 148
Zigmond, M. J.Burke, R. E. 2002 Pathophysiology of Parkinson's diseaseNeuropsychopharmacology: The Fifth Generation of ProgressPhiladelphiaLippincott Williams and Wilkins1781