week 9 – mar 12 and 13 2014 neural basis of the cockroach ... · neural basis of the cockroach...

12th March 2014 Bio 335 - Animal behavior - Week 9 - Lecture 17 1

WEEK 9 – Mar 12th and 13th 2014Neural basis of the cockroach escape behavior

Raghav RajanBio 335 – Animal Behavior

Mar 12th 2014


Case study – cockroach escape response

● Cockroaches reliably escape from predators● One such predator is the toad and cockroaches

escape from the toad's tongue


How does the cockroach escape the toad? Proximate question

● Careful analysis of videos of toad striking at a cockroach (64 frames/s)

● Initially roach pivots away and then runs

● Similar to response to gusts of wind

http://faculty.bennington.edu/~sherman/neuro/escape%20cockroach%20toad.pdf


More proximate mechanisms

● Giant interneuron that mediates response

● Cerci have about 220 hairs

● Each hair is hinged such that it can move in one of two directions (180 deg. apart)

● Different hairs move in different directions

http://nelson.beckman.illinois.edu/courses/physl416/ventralNerve.html

http://nelson.beckman.illinois.edu/courses/physl416/ventralNerve.html


How does the cockroach escape the toad? Proximate question

● Careful analysis of videos of toad striking at a cockroach (64 frames/s)

● Initially roach pivots away and then runs

● Similar to response to gusts of wind

http://faculty.bennington.edu/~sherman/neuro/escape%20cockroach%20toad.pdf


Questions about the proximate mechanisms

● Cockroaches normally walk around and predators find moving prey easier to locate – how does the cockroach get around this?

● How does the cockroach sort out false alarms from real stimuli

– Self-movement will also result in changes in the wind

– What if there is a breeze in the environment● How do the cerci detect wind?● How do they signal the precise time of a stimulus?● How do they signal the direction of the wind?● How do downstream neurons read this code?● How do downstream neurons use this information to plan the

appropriate behavior – pivot and run?


Experimental setup to study walking cockroach

● Cockroach restrained in such a way that it could move its legs

● Tube positioned to provide puff of air

● Leg position monitored with photocells


Apparatus used to deliver air puffs at different angles

● Solenoid valve striking a rubber membrane


Walking cockroaches also respond to air puffs

● Top trace – wind recorded inside puff tube

● Bottom two indicate leg movements

● A (2.6m/s wind puff elicits running)

● B – 3mm/s elicits a change in stepping about 50% of trials (90% involve pause)

● C – 12mm/s elicits run


Response latency is lower during slow walking

● Low wind – 25mm/s

● High wind – 2.6m/s

● Response latency as low as 14 ms

● All neural processing has to occur in this 14ms!


Now, how does a walking cockroach sort out real stimuli from false alarms

● Walking will induce air flow in the opposite direction● Stepping will induce air flow gusts near the cerci● Hypothesis: Maybe the cockroach uses a different cue

– acceleration and not velocity of air puff to sort out real stimuli from false alarms

● Predictions:

– Velocity might be comparable for air flow gusts induced by stepping and toad

– But acceleration is different● Built apparatus to delivery wind at different

accelerations but similar velocity


Apparatus to vary acceleration and velocity

● Electromagnet switched from DC to AC to start drop● Acceleration increased by increasing mass● Velocity increased by increasing distance over which the mass

dropped


Cockroaches can still detect 3mm/s air puffs

● Pause on 45% of the trials with 3mm/s air puffs despite headwind of 80mm/s


Leg gusts – fluctuations in the wind elicited by leg movement

● Measured near both cerci● Periodic fluctuations that are in sync with leg● Fluctuations on both sides are out of sync with

each other, just like the respective legs


Analysis of accelerations during leg gusts and air puffs are different

● Leg gusts rarely reach above threshold acceleration

● Acceleration caused by leg gusts greater at higher walking speeds

● But, at higher walking speeds, thresholds for pausing are higher


Escape response is dependent on acceleration cues

● Pk velocity – 40mm/s in all cases

● A – acc – 1500mm/s2

● B – acc – 320mm/s2

● C – acc – 40mm/s222


Wind acceleration appears to be the cue used

● Pk velocity – 40mm/s for all stimuli

● A – wind from behind (No headwind)

● B – wind from behind (with headwind)

● C – wind from 90deg. on the right

● D – wind from front● C and D – no headwind


Summary of behavior

● Cockroaches most sensitive to stimuli during slow walking

● Escape latency can be as low as 14ms● Wind acceleration appears to be the cue used● Now, how does the nervous system detect this and

generate the appropriate response● First step – anatomy


Nervous system of the cockroach


Escape circuit


Structure and response of sensory neurons in the cercus

● Each cercus has about 220 filiform hairs – receptor neurons

● Each hair is hinged such that it responds to only two directions (180 deg. apart)

● Different hairs respond to different direction pairs


Quantifying the response on a polar plot

● Angle relative to the midpoint between the two cerci

● No of spikes is plotted as the radius

● 0deg. wind from behind the animal

● 90L – wind from animal's left to right


Direction selective response of a sensory neuron

● No. of spikes plotted vs. direction of wind stimulus

● 0deg. wind from behind the animal

● 90L – wind from animal's left to right

● Acc. and velocity are very high – what is it like with near threshold stimulation?


Different cells have different tuning curves


Sensory neurons response latency is about 9ms

● Air puff is about 20ms in duration (rising phase)

● Spontaneous activity is around 5 Hz (0-61Hz)


Responses of giant interneurons

● Same apparatus used to generate stimuli

● Recording of air puff

● Intracellular recording from giant interneuron

● Extracellular recording from whole nerve cord


Position of giant interneurons

● Atleast 7 giant interneurons on each side in the ventral nerve cord


Most GIs show direction-selective responses

● Direction cannot be computed unambiguously from the activity of any individual GI


GI responses have high firing rates and are fast


Latencies to first spike in all the GIs are small

● Suggests that there definitely is sufficient information to generate escape movements


How does direction selectivity arise in the GIs?

● They get both monosynaptic and polysynaptic input from the cercal sensory neurons

● Since cercal sensory neurons are direction selective, they could entirely be the source of direction selectivity in GIs

● Are they entirely the source of activity for GIs?


Removal of ipsilateral input reduces direction selective responses in some GIs


Origin of direction selective responses in GIs

● The previous result suggests that bilateral comparisons are not involved

● Rather, direction selective responses might arise purely from the direction selective responses of the cercal sensory neurons


Lesions of different GIs perturb escape behavior to different extents


Now what aspect of the spike trains of GIs are involved in determining escape direction?

● Wind from the right● GIs on the right fire more spikes (~ 13 more spikes)● GIs on the right fire spikes earlier than GIs on the

left● GIs on the right have more complex temporal

patterns (bursty)● Now which aspect of these features is used by

downstream neurons to determine escape direction?● Correlation vs. causation and what is the code?


Electrical stimulation to establish causation

● Can stimulate the axon of a GI and evoke spikes


Example of experiment with electrical stimulation and wind stimulation


Electrical stimulation of long duration makes the cockroach turn into the wind stimulus

● Wind always delivered from the right

● Here, left GI was stimulated

● Left GI fires first● Also fires more

spikes● But right GI is

more bursty● Temporal pattern

doesn't seem to be important


Reduce evoked spikes – so now left GI fires first, but fires less number of spikes


With weaker electrical stimulation, turn direction is not changed

● Wind stimulus from the right● So, that suggests that the relative number of

spikes is the important cue● Although left GI fired before right GI, the cockroach

still turned to the left● Right GI fired more spikes than the left GI● So, relative number of spikes might be the

important factor


So how do the different GIs contribute to determining the escape direction

● Winner-take-all – whichever GI fires the most, that GI determines the direction completely

● Population vector – all GIs continue to contribute to the decision, but in proportion to the number of spikes they produce


Cockroach escape system

● Robust escape system that is used to detect wind-based threats

● Activates a complex pivot and run response● Giant interneurons with large diameters ensure fast

conduction velocity and low latency● Comparisons between right and left used to determine

direction of turning (not amplitude of turning)● Difference in number of spikes between left and right

may be used to determine direction of stimulus● Different GIs with different direction tuning appear to

contribute towards determining direction of stimulus


Two different mechanisms to generate selective turns

● Cockroaches can detect 15deg. left of “head on” and 15deg. right of “head on” accurately (~90% of the trials)

● But, cercal neurons and GIs have broad tuning – so far no neurons with such narrow tuning have been discovered

● Either such neurons exist but have not been discovered● Or, they don't exist

– Instead when wind is from the left, both left and right GIs are activated (right GIs a little less)

– Stronger muscle contractions for the right would over-ride the left turn


Testing the two hypothesis

● Studied the coxal-femoral joint during wind presentations from 15deg. left or 15deg. right

● Closer and opener muscles activated at different times


Joint opening and joint closing recruit the muscles alternatively and not together


Cricket cercal system – very similar to the cockroach cercal system

● Mediates escape responses in the cricket

● GIs are similarly broadly tuned

● But crickets appear to detect wind direction with high precision

● Hypothesis – synchronous spiking between GIs sharpens tuning


Greater synchrony between GIs for specific directions

● Synchrony is direction-dependent

● Cross-correlation – the probability of one neuron spiking given a spike from the other neuron


Synchronous firing sharpens tuning curves for wind direction

● Sharper tuning curves● Make it plausible that

synchrony between GIs is a means for detecting wind direction accurately


New pieces to the puzzle


New pieces to the puzzle

● Escape trajectories have some variability – for a given direction of wind, the cockroach chooses one of 3 or 4 different escape trajectories – confuse predators with some uncertainty!

● Escape circuit is flexible● Touch, antennae can also trigger escape through the same

circuit● Ablating all the giant interneurons does not abolish behavior –

instead it reduces the occurences of turning

– When there are responses, the direction and magnitude of turning is comparable to normal cockroaches

– Only the latency is longer

– Suggesting of a non-GI escape circuit too


Escape circuit – fast, but flexible

● Adding a little unpredictability to confuse the predator


General principles from studying the escape system

● Escape responses need to be fast – often, bigger axon cells with faster conduction velocities

● Conserved circuitry across insects mediates fast escape response

● Escape circuit is fast, but remains flexible● Specialized sensory cells● Population code for direction – vector averaging

– Robust and exhibits some plasticity after cercus loss● Possible code with synchrony between neurons

week 9 – mar 12 and 13 2014 neural basis of the cockroach ... · neural basis of the cockroach...

Documents