Juvenile Homing Strikes: Sensory Decoding, Motor Pattern Selection & Innate Knowledge

see Parichy et al. 2009

Zebrafish Stages

Rebecca E. Westphal (North Shore Community College, Lynn MA) and Donald M. O’Malley (Northeastern University, Boston MA)

Increased Performance

Conclusions: (1) Late Larvae are freed from the constraints of early larval routines. (2) LL randomness is akin to Mammalian “play”? (3) Reward and Basal Ganglia systems likely contribute to emergence of JHSs.

Maturation of Zebrafish Prey Capture

Key QuestionsInnate Early Larval Behaviors – How has evolution stored object recognition, serial decision-making and distinct motor programs (J-turns, slow swims, capture swims) in the zebrafish genome?

How are Late Larvae Freed from Evolution’s Dictates? – After two weeks, automaton larval programs are overridden, although they may still be flexibly incorporated into compositional predatory schemes.

How are infinitely-varied predatory episodes produced? – During the transitional late-larval stage, ZF use an increasingly diverse set of predatory episodes, including variations of elemental maneuvers and extremely varied maneuver sequences.

Are Zebrafish Intelligent? – While early hominids spent 2 million years banging rocks together, zebrafish, within 4 - 5 weeks, demonstrate great computational and motor prowess and vastly better survival skills than 1 month old primates.

Juvenile Homing Strikes – How are extremely diverse and exquisitely efficient strikes computed and implemented by juveniles and adults? This poster suggests that emerging (developing) motor skills (via Basal Ganglia and Cerebellar maturation), in conjunction with early innate knowledge, provide a means for the emergence of strategic computations and implementation of highly varied and sophisticated strike strategies. Conventional error-correction based motor learning strategies do not seem sufficient to account for JHSs.

Westphal and O’Malley, 2013, FINS

Early-Larval Prey Capture Juvenile / Adult Homing StrikesStaccato, long duration episodes Continuous, short duration3 distinct maneuvers, w/ pauses Extremely diverse motor patternsSerial decision-making; iterative Pre-computed trajectories & maneuversAccurate, close range strikes Superb Accuracy, distant strikesInnate O.R. & motor programs Innate K. or Fast Motor Learning?

Reflections for Aficionado’s & Savants

- How does evolution store “New Knowledge” in the genetic code?

Ancestral predators likely used turns and forward swims long before the complex features of J-turns and Capture Swims were invented. How was this new IK (innate knowledge) stored in the ZF genome, along with O.R. (object recognition, of suitable prey), serial decision making (e.g. young larvae can reject Artemia) and winner-take-all (WTA) computations, where e.g. one prey item must be selected and responses to other prey suppressed (see Fajardo et al., 2013). Quite a number of groups are investigating the neural controls of early larval prey capture and visual info processing (Niell and Smith, 2005; Gahtan et al., 2005; Del Bene et al., 2008; Douglass et al., 2008; Orger et al., 2008; Naumann et al, 2010; Bianco et al., 2011; Green and Hale, 2012; McClenahan et al., 2012; Ahrens et al., 2013; Patterson et al., 2013) but we are interested in what genetic changes enabled these specific behaviors to be added to the ancestral developmental scheme and genome.

- How many bits of information are required for O.R. by larval ZF?

McDonnell et al. (2011) report that 35 or 44 bits per second can be reliably transmitted along an axon (given their model parameters), and so I would like to know how many bits are required for larval ZF to recognize a prey item (or predator, where an escape can be initiated in 4 msec). This will likely depend upon the coding and O.R. schemes, but specialized cells (ala Niell and Smith, 2005) should make O.R. easier, wherein any given patch of retinorecipient optic tectum can distinguish prey from many other items via size and relative movement.

- Nature vs. Nurture Zebrafish Style: Serial Emergence of Innate Capabilities?

Early larval predation is entirely “nature” in that no prior experience is necessary for highly-successful, well-formed strikes. The rapid advance of ZF strike capabilities might be due to developmental learning (niche nurture), but if the learning space is too large (i.e. effective solutions too rare), many ZF will die. The complexity of the solution space and the high strike accuracy seen across ontogeny together suggest an evolutionary boost to larval performance, enabling rapid emergence of JHSs. [Asides: Can the niche be seen as playing an instructive role to train ZF and other animals? Does Tenenbaum address innate contributions to human IQ?]. While the implementation of complex, yet selectable innately-stored motor programs might seem unlikely, the fine axial motor control of early larvae (Borla et al., 2002) shows that this may be possible.

E = Episode S = Strike

Neural Coding Operations

Early Visual Processing – motion & object detection, visual coordinates DSGC signals, tectal object segmentation, directionality/coordinates early-lzf: left/right discrimination. late-lzf: angle estimation

Neural Decision Making – early-LZF: (1) prey O.R., (2) J-turn or SS, (3) Cswim/strike on “contact” late-LZF: (1) prey O.R., (2) calculate J-turn or RT angle, (3) close & strike coding in Late Larvae is needed to produce: -- major scythe or little -- single bend or 7 cycle swim -- backing and diving -- etc. etc. Juveniles employ strategic computation (emerges in Late Larvae)

Applicability of Popular Computational Approaches?

Shannon Information Theory– no evidence yet for Shannon compression or code modification to maximize channel capacity during Prey Capture (PC).

Mutual Information / Entropy – if communication channels not near capacity, then noise considerations / signal corruption might not factor into PC info processing.

Grandmother Cell Coding– dedicated circuits likely play key roles, especially in early larvae (Liu and Fetcho, 1999; Orger et al., 2008); possible means of embedding Innate Knowledge / Universal Physics in CNS. Sparse Coding fits with such schemes.

Distributed Codes– widespread evidence in zebrafish and lamprey of widely distributed processing of sensory signals (Zelenin et al., 2001; Gahtan et al., 2002). But distributed and dedicated codes seen incompatible.

Bayesian Inference – Specific optimal decisions may have been learned over evolutionary time and this knowledge integrated into zebrafish genome. ZF brains presumably cannot actively represent P values and compute with them.

Coding and Computation of ZF Prey Capture

A. Receptive Field of single tectal neuronB. display of RFs of neurons across tectumC. RF diameters (but cells respond better to smaller objects)D,E. topographic oz. of tectal neuronsBELOW: cluster analysis of large population of tectal neurons.

Neuron 45:941–951, 2005

Population Recording in Zebrafish Optic Tectum by Niell and Smith, 2005

Descending Motor & Spinal Systems

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=

How do brainstem neurons control spinal circuits to create diverse motor patterns?

Brain StemBrain Stem

Spinal CircuitrySpinal Circuitry

sophisticated,extensivelocomotorrepertoire

two animals enter, one animal leaves

Descending Neurons

Juvenile Homing Strikes

25 um

A B

C D

M

M

Midbrain

Rostral Spinal cord Mid-Trunk Spinal Cord

Larval Zebrafish DMCS & Spinal Cord

- What new capabilities come on line in Late Larval Prey Capture? Freedom, Precision & Fusion

Early larval ZF make rote use of canned maneuvers (J-turns, slow swims and capture swims). Within a few weeks, larvae exhibit diving, vigorous backwards swims, non-SS forward swims, merged-turn/swim behaviors, long and unusual sequences, contorted maneuvers and extremely varied means of striking at Artemia. While these episodes fall well short of JHSs (Westphal and O’Malley, 2013; FINS) they foreshadow the flexibility and fusion exhibited by juvenile and adult zebrafish. This late larval “freedom” from earlier constraints implies an ability that is both exploratory and compositional.

- How are maneuvers merged and angles computed?

Late larvae can conjoin forward swimming and turn maneuvers into single movement bouts, which means they have escaped the earlier requirement to select ONE behavior, pause, then select the NEXT behavior. If sensors suggest they should both TURN and MOVE CLOSER (by virtue of tectal activation indicating the need for both), the weaker signal is not canceled: instead a turn is implemented and motion continues as forward swimming. This may be enabled by better sensory computations (calculating angle AND distance) and by the ancestral basal ganglia directing the sequence (perhaps with the help of persistent neural activity in brainstem). Early optic tectum may utilize inhibitory paths that accomplish WTA of one action (turn vs. swim) by suppressing the weaker need, whereas late larvae may store the additional information. It also appears that more precise turns are now made at the outset of episodes, i.e. large initial turns (RTs) are often seen that approach proper orientation (whereas early larva J-turns are more repetitive and iterative in their angle homing).

- How many GENES are required?

It is unknown how the newly exhibited capabilities are acquired, i.e. the contributions of motor learning or the emergence of new behaviors from ongoing developmental processes. Human brains are so complex and capable of learning so many different things, that we cannot simply specify each capability with a gene: the number of genes is vastly fewer. However, what genes CAN do is constrain the solution spaces to problems and provide organisms with stored motor programs and knowledge (like fears of snakes and cliffs). While some genes can be used to construct general purpose learning algorithms (within e.g. neocortex and hippocampus, apparently), other genes must, at least in zebrafish, specify the object recognition, serial decision making and stored motor programs. Such specification (dedicated circuits) can greatly constrain the solution space of ecological problems (such as hunt faster). Such constraints must, of necessity impose limitations, but late larvae seem quite flexible and compositional. The genetic and neural circuit basis of this rapid emergence of predatory capability is quite relevant to understanding mammalian systems and indeed human intelligence, given the many conserved aspects of vertebrate brain structure and the abysmal understanding we have of mammalian systems.

Sensory Contributions to Strike Accuracy

Late Larvae: Behavioral Maneuvers Summary [LL Stage = transition from EL to Juveniles]

FISH SEQUENCE DESCRIPTION SUMMARY COMMENTSApr3Feed8 J-turns, then multiple C-swim like bouts, quasi-continuous long episodeApr3Feed16 Long series w/ strong C-swim like bouts w/ course corrects: due to prey mvmt.; long distanceF017.20F5 J-bend, J-bend w/merged SS, mild 2-bend SS, mild strike no scythe in strike, tiny pausesR017.20F2 looks like early lzf. Backs after 1 turn; BIG strike acceler. [check to see if he dives]R018.21F1 After Arty drops: Big RT, min. RT, moder. RT, 4th small RT aligns well uses RTs no J-turnsR018.21F2 Big rRT, weak SS adjusts rt, SS adj. left, mild 6-bend strike last 3 bends strongerR018.21F3 2 JTurns, two SSs, wicked accel. in CswimR018.21F4 approx. 9 small discrete mvmts (turns, SSs), vigor strike long complex manu. at f800R018.21F5 contin. asymm fwdSwim w/Δs direction; great quick Scythe from rest backs 3x and divesR018.21F7 long series of SSs across dish and SS-like strike; long init. pause seems doped upR018.21F8 RT, SS, 2nd RT w/SS-bends, then leftRT, 3bSS, backs up, 6bSS dives/strikes complex strike w/JT & scytheR018.21F9 Artydrop, turn @55fs, 2 SSs, RTw/bent-7bendSS, dbl scythe contortional? held bends? R018.21F11 80deg. 2bRT, asymm2bSS, SS-like strike w/Sbend straight on impact; dbl clutch?R022.20F good init. J-turn, normal strike (misses? post strike action?) engulfment not clearR022.20F2 successive backups as Arty approaches, JT, SS, dive, 9bSS-strike mild bends in strike; backing precedes dives

Fixed Routines are Disrupted in the Transitional Period

Loss of Early Larval (EL) fixed behavioral routines might be caused by activation of Basal Ganglia circuitry, but by itself this seems insufficient to account for highly varied use and sequences of different maneuvers used in EL prey capture and other behaviors.

Role of Neural Systems in ZF Prey Capture

Retina and Optic Tectum– primary means for selecting attack strategies / computing turns, initiating action. [See citations in Westphal & O’Malley, 2013 + info on Lateral Line inputs]

Basal Ganglia– Ancestral basal ganglia of ZF might initiate & sequence distinct maneuvers in LL & juveniles (although see Borla et al., 2002 re: FAMC in larvae).

Cerebellum– is active in larval learning (Bae et al., 2009; Aizenberg and Schuman, 2011) and must contribute to general motor coordination, but error-correction of faulty prey strikes seems unlikely to account for JHSs.

Evolution / Development– Evolution has (perhaps) performed Bayesian selection for optimal decision makers and possibly stored great amounts of world knowledge and decision sequences in the genetic code (source code), which is expressed via development as dedicated neuronal circuits (compiled code).

ZF Learning Systems— Motor Learning (Portugues and Engert, 2011; Ahrens et al., 2012), Cerebellar Learning (Aizenberg and Schuman, 2011) and Operant Learning (Valente et al., 2012).

Dopaminergic Neurons in ZF embryo. From Holzschuh et al. 2001; Driever Lab. In Mechanisms of Development.DC = Diencephalic cluster: 6 cells to 50 cells (in 20 72 hrs.).