Topics Analysing behaviour • Acoustic Startle – jumping when some one says “BOO” • Decision – widely studied in many taxa • Perception • Categorical Perception • Easy to talk about, but what exactly do you – continuous variable perceived as discrete mean? categories – If you make a clear and strict definition, it may • Selective Attention include things you don’t expect. – focus on one signal among many – Next week

NROC34 2012:3 1 NROC34 2012:3 2

Cricket Auditory System

Ultrasound Hearing in Crickets

Just what is AN2 doing if it’s not so important for communication?

ON1, AN1 and AN2 all receive direct input from auditory receptors. NROC34 2012:3 3 NROC34 2012:3 4

1 Int-1 & AN2: needless confusion AN1 & AN2

German name: American name: Int-1

5kHz

ultrasound

(also ipsi- vs contralateral) low

high Segregation of frequency bands in central auditory pathway. NROC34 2012:3 5 NROC34 2012:3 6

Counter-measures against Why ultrasound? echolocation

Bats eat many . Night-flying insects are vulnerable to . Many have They hunt by echolocation - evolved the ability to hear the the production of ultrasonic echolocation calls of bats as sound pulses that are an early warning system. reflected by objects in the Hearing ultrasound causes environment. These echoes these insects to take evasive of their own cries allow bats action. Crickets are amongs to detect and localize prey. those that hear and avoid ultrasound.

Lacewing avoids being eaten. NROC34 2012:3 7 NROC34 2012:3 8

2 Startle Response Praying Mantis

Eunemobius carolinus

NROC34 2012:3 9 NROC34 2012:3 10

Flying phonotaxis

But the reason they in the first place is to go where there are other crickets. So they must have two responses to sound while they are flying: Steering response of flying Positive Phonotaxis in crickets... response to the songs of other crickets; Negative Phonotaxis in Moiseff, Pollack, Hoy (1978) PNAS response to ultrasound. 75(8):4052-4056

Tethered flying (the Polynesian cricket, ). NROC34 2012:3 11 NROC34 2012:3 12

3 Positive and Negative Sensitivity and Discrimination

Steering movements during flight. Direction vs frequency turn Threshold curves Positive for frequencies that excite AN1, negative for frequencies that spkr AN1 AN2 excite AN2. No Sound Song (5kHz) Ultrasound (40kHz) NROC34 2012:3 13 NROC34 2012:3 14

Methods

Initiation of behavior by single neurons.

Nolen and Hoy (1984) Science

226:992-994 Cricket is dissected for Record from Int-1 (AN2) intracellular recordings, middle- (intracellular) and from dorsal and hind legs removed. Flight longitudinal muscles (extracellular). behaviour indicated by rhythmic Stimulate with ultrasound. viration of wing-stumps.

NROC34 2012:3 15 NROC34 2012:3 16

4 Correlation and context Sufficiency

>220 sp/s AN2 is excited by ultrasound. If it responds vigorously (>220 spikes/sec) then a steering response always occurs if and only if the is flying. The stronger the AN2 response, the stronger the steering response. DLM response A context-dependent correlation between the behaviour and <220 sp/s activation of neuron.

Excite AN2 in the absence of ultrasound and the same pattern is observed. DLM activity is elicited if AN2 fires >220 spikes/sec. AN2 response (spikes) Used anode break to excite neuron = sudden release of hyperpolarization. NROC34 2012:3 17 NROC34 2012:3 18

Necessity AN2 excitation

ultrasound DLM excitation (via brain etc.)

hyperpolarize AN2 - no DLM excitation Categorical perception of sound frequency by crickets

Wyttenbach, May, Hoy (1996) back to normal Science 273:1542-1544

NROC34 2012:3 19 NROC34 2012:3 20

5 Habituation/Dishabituation Again Categorical Perception

• distinct categories with sharp boundary • no discrimination within categories • peak discrimination at boundary • close agreement between labelling and discrimination

If test stimulus dishabituates, response to probe should be greater than response to last of habituating series.

NROC34 2012:3 21 NROC34 2012:3 22

Labelling and Discrimination

e.g. Ba/Pa

Voice onset time - continuous variable, but perception is categorical

NROC34 2012:3 23 NROC34 2012:3 24

6 Within and between categories Two kinds of sound for a cricket • high or low frequency • DANGER – cricket is flying – ultrasound – Int-1 (AN2) excited > 220 spikes/sec • CONSPECIFIC – walking or flying – audio (near 5kHz) – 30 Hz pulse (syllable) rate

NROC34 2012:3 25 NROC34 2012:3 26

Putting it all together Only positive phonotaxis: slow What next?

recognise Temporal filtering • More hearing localise Side-to-side Motor Output comparison – e.g. selective attention: how to find a single individual in the midst of many suboesophageal ganglion • Vision AN1 fast AN2 – motion detection – pattern recognition Peripheral Filtering: frequency; direction Contrast enhancement; frequncy coding NROC34 2012:3 27 NROC34 2012:3 28

7 ochracea directional hearing Mechanics, coding and attention: why everyone should be interested in • Acoustic . • Mechanics: Physical basis of directional hearing • Coding: how is directional information aka Directional hearing in Ormia encoded by the auditory system? ochracea • Attention: In the “real world” there may be many crickets.

NROC34 2012:3 29 NROC34 2012:3 30

Ormia is a . Parasites need hosts

NROC34 2012:3 31 NROC34 2012:3 32

8 Ormia ochracea directional Phonotaxis hearing

• Acoustic parasitoids: fascinating, but how is that physically possible? • Mechanics: Physical basis of directional hearing • Coding: how is directional information encoded by the auditory system? • Attention: In the “real world” there may be many crickets. NROC34 2012:3 33 NROC34 2012:3 34

The Size Problem Cricket song

t = very small

I = very small

5 kHz tone pulses 10 ms pulse duration 20 ms pulse period 1 ms rise/fall times (cos2)

NROC34 2012:3 35 NROC34 2012:3 36

9 Auditory system Auditory system

cuticular bridge tympanal membrane

sensory organ Cuticular bridge afferent nerve Tympanal to CNS membrane midline

NROC34 2012:3 37 NROC34 2012:3 38 Robert et al. 1992, 1994

Two modes of vibration 3

1 2 Symmetric

Anti-symmetric

123 Acoustic stimulation excites both in different proportions, depending on angle of incidence: linear summation of the two modes…

NROC34 2012:3 39 NROC34 2012:3 40

10 Two directional effects on tympanal Ormia ochracea directional motion hearing

5 kHz • Acoustic parasitoids • Mechanics: physically possible Amplitude difference – max. 10 dB • Coding: how is directional information encoded by the auditory system? • Attention: In the “real world” there may be many crickets.

Contralateral delay – max. 55 µs Miles et al. 1995 RobertNROC34 et al. 2012:31998 41 NROC34 2012:3 42

Telling right from left 50 %

50 %

NROC34 2012:3 43 NROC34 2012:3 44

11 This method didn’t work.

100

10 90

80

70

Correct turns (%) 60

50

0 5 10 15 20 25 30 Angle of incidence (degrees)

NROC34 2012:3 45 NROC34 2012:3 46

0º 0º -10º 10º -10º 10º

10º 10º

-10º -10º

Mean path of Mean path of ten responses ten responses NROC34 2012:3 47 NROC34 2012:3 48

12 Graded turns Lateralization

-1º 1º

1º 4º 2º 0º 6º 10º n = 7 flies, 10 runs/angle/fly

Proportion correct Proportion n = 19 flies, 20 runs/angle/fly

20º Angle of incidence (degrees) spkr left left right spkr right Turn size (degrees) size Turn o = correct mean paths (n = 10) for NROC34 2012:3 Speaker azimuth (degrees) 49 NROC34 2012:3 50 one fly x = incorrect

Directional responses of auditory Directional Acuity receptors

• Extremely accurate • Miniscule sensory cues: for sound incident at 2º, ITD at the eardrum is only 50 nanoseconds. – Mechanical system is very sensitive – How does a simple nervous system read this?

NROC34 2012:3 51 NROC34 2012:3 52

13 Unusual response properties 6.0 Timing of an afferent spike Ipsilateral Sound shifts with sound intensity. 5.0 Contralateral Sound

phasic, low jitter 4.0

3.0

Response Latency (ms) Latency Response 2.0 60 70 80 90 100 Stimulus Intensity (dB/SPL) Timing of population response will also shift with intensity.

A population of spikes from each ear. Frequency (Amplitude) Frequency (Amplitude) Timing of receptor spikes could be basis for directional Latency (Time) hearing. OshinskyNROC34 &2012:3 Hoy 2002 Latency (Time) 53 NROC34 2012:3 54

2. Receptor latency 1. Tympanal vibration amplitude - mean latency difference - intensity difference 0 6.0 330 30 10 Ipsilateral Sound 5 5.0 Contralateral Sound 0 300 60 -5 4.0 -10 -13 270 9 3.0 -8

-3 (ms) Latency Response 2.0 2 240 120 60 70 80 90 100 Stimulus Intensity (dB/SPL) 7 12 210 150 180

t 3. Difference in mean latency of summed responses of each ear. Amplitude (or frequency)

NROC34 2012:3 55 NROC34 2012:3 56 Time

14 Relative timing shifts with speaker Relative latency encodes direction position

Spkr left

200 s) Left ear μ 100 Right ear y1 0 3.5 µs/° Spkr right -100 −200 −100 0 100 200

Latency difference ( difference Latency -200 Left-right,−50 Mean 0 ± SE, n 50 = 11 x1 -100 -50 0 50 100 Speaker azimuth (degrees)

Time NROC34 2012:3 57 NROC34 2012:3 58

Ormia directional coding Very impressive • Relative latencies of receptor spikes from each ear can encode sound direction. Once more, the Master Designer has taught the best of human designers some lessons. Sadly, the main research • At smallest angles interaural latency paper called the fly’s ear an ‘evolutionary innovation’, differences < 10 µs. without the slightest explanation of how the mechanical – Better than 50 nanoseconds, but still not much structure and nervous coding system could arise by small mutations and natural selection.

Creation Ex Nihilo, 23(4):54-55

NROC34 2012:3 59 NROC34 2012:3 60

15 …and useful, too. Novel mechanism of acoustic Real Ormia ear directionality, with applications…

Ormia-inspired microphone Simulated response of microphone diaphragm modelled on fly eardrums.

Ron Miles, Binghamton University NROC34 2012:3 61 NROC34 2012:3 62 http://research.binghamton.edu/faculty/miles.htm

…both benign… …and sinister.

NROC34 2012:3 63 NROC34 2012:3 64

16 Where does this lead? Emblemasoma sp. • Biomimetic technology: miniature directional microphones based on principle of Ormia eardrum have potential for very high acuity • But - in Ormia performance depends on highly specialized auditory coding (tailored to specific signals). • Also - effects of noise unknown (flies seem to deal with it, so that is promising at least).

NROC34 2012:3 65 NROC34 2012:3The answer lies in more basic biological research. 66

17