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1 doi: /nture10754 Supplementry note 1 To ompre our dt with previous studies, we mesured the width of spikes from identified dopminergi neurons nd unidentified neurons from DATCre mie. Previous studies used riterion tht dopminergi neurons should hve wide spikes. We found signifint diversity in spike wveforms from identified dopminergi neurons (Fig. S4). There ws no signifint differene ross neuron types in spike durtion (ANOVA F 2,89 = 0.15, P > 0.7). We found tht Type I neurons (nd identified dopminergi neurons, when onsidered seprtely) hd lower seline firing rtes thn Types II or III neurons (Type II Type I men ± 95% CI, 6.73 ± 6.72 spikes/s, Tukey HSD test, P < 0.05; Type III Type I, ± 8.84 spikes/s, P < 0.01), lthough mny Types II nd III neurons hd low firing rtes (<10 spikes/s). Thus, mny identified dopminergi neurons in the present study would hve een missed using previous riteri. Supplementry note 2 Models of RPE typilly ssume two exittory inputs, those from rewrdprediting ues (CS) nd those from rewrd (US), in ddition to inhiitory inputs refleting rewrd expettion disussed ove (Fig. S12). Where do these exittory inputs ome from? Tht some dopminergi neurons respond preferentilly to rewrd (nd wekly to CS) rises the possiility tht these USpreferring neurons my provide other CSpreferring dopminergi neurons with the rewrd signls. If this is the se, these neurons should meet the following preditions. First, exittion of these neurons should use phsi exittion of other dopminergi neurons (the ones lulting RPE). Seond, these neurons should not reeive inhiitory inputs enoding rewrd expettion. First, we oserved tht the exittion of dopminergi neurons (using ChR2 stimultion in DATCre mie) did not use synpti exittion of dopminergi neurons (Fig. S6d). This result does not support the view tht lss of "rewrdoding" dopminergi neurons exites other "RPEoding" dopminergi neurons. Seond, the mgnitude of inhiition during rewrd omission ws s lrge in USpreferring dopminergi 1
2 neurons s in CSpreferring dopminergi neurons (Figs. 4, S8, S9). This does not support the view tht there is lss of dopminergi neurons tht purely enodes rewrd signls. These results suggest tht rewrdenoding neurons, s proposed in the models, re loted outside the. Similrly, lthough CSpreferring dopminergi neurons n, in priniple, provide exittory inputs to other dopminergi neurons, our results do not support this view, suggesting tht exittory inputs for CS lso ome from outside the. Supplementry note 3 Our experiments llow us to mp neuron's funtion onto the trnsmitter it releses. The perentge of Type I neurons (49/95, or 52%) is lose to the estimte of the perentge of dopminergi neurons in rt (5565%) 68. Furthermore, the unidentified Type I neurons showed similr tskrelted tivity to identified dopminergi neurons (Fig. S11,). Together with the oservtion tht Type I neurons, ut not Types II nd III neurons, responded to light stimultion in DATCre mie, this suggests tht unidentified Type I neurons were lso dopminergi (lthough we nnot rule out the possiility tht some Type I neurons were nondopminergi). The seond experiment showed tht identified GABAergi neurons were of Type II. The identity of Type III neurons remins to e determined. They my relese different neurotrnsmitter, suh s glutmte 14, ut we nnot rule out the possiility tht Type III neurons re GABAergi or dopminergi (lthough the ltter seems unlikely, given the high effiieny of ChR2 expression in dopminergi neurons throughout, regrdless of projetion trget; see Figs. S2, S3). 2
3 doi: /nture10754 r 1 r 2 Density Firing rte (spikes/s) r 1 d r 2 Firing rte (spikes/s) Density Firing rte (spikes/s) P(r 1 > riteri) uroc = 0.88 Time odour (s) uroc = P(seline > riteri) e uroc P(r 2 > riteri) P(seline > riteri) Time odour (s) uroc (vs. seline) 1 (Inrese) 0 (Derese) Figure S1. ROC nlysis., Rster plot from 15 trils of 149 igrewrd trils from dopminergi neuron. r 1 nd r 2 orrespond to two exmple 100ms ins., Averge firing rte of this neuron., Are under the reeiver operting hrteristi urve (uroc) for r 1, in whih the neuron inresed its firing rte reltive to seline. We ompred the histogrm of spike ounts during the seline period (dshed line) to tht during given in (solid line) y moving riterion from zero to the mximum firing rte (in this exmple, 68 spikes/s). We then plotted the proility tht the tivity during r 1 ws greter thn the riteri ginst the proility tht the seline tivity ws greter thn the riteri. The re under this urve quntifies the degree of overlp etween the two spike ount distriutions (i.e., the disriminility of the two). The histogrm in the top pnel is trunted t n ordinte vlue of 0.2 for disply purposes. d, Similr to (), ut for r 2, whih orresponds to n uroc vlue lose to 0.5 (i.e., tivity lose to seline). e, uroc response profile for the full durtion of the tsk, with r 1 nd r 2 indited y rrows. Shown elow re the het mp vlues, s depited in Fig
4 doi: /nture10754 DATCre DAPI TH ChR2EYFP VgtCre DAPI TH ChR2EYFP GAD65/67 ChR2EYFP TH % neurons 100 d 0 % ChR2EYFP mong TH neurons 50 µm ChR2EYFP GAD65/67 TH Figure S2. Effiient nd speifi expression of ChR2EYFP in dopminergi nd GABAergi neurons., Blue: DAPI (nuler mrker). Red: immunostining for TH (dopminergi neurons). Green: ChR2EYFP. Sle r is 50 μm., Colors s in ; White: immunostining for GAD65/67. Slies re from DATCre () or VgtCre () mie injeted with raav5chr2eyfp., Perentge of neurons leled for EYFPChR2 nd TH (n = 666 neurons in 2 mie). d, Perentge of neurons leled for EYFPChR2, TH nd GAD65/67 (n = 433 neurons in 2 mie). 4
5 doi: /nture10754 stritum d Distne from midline (mm) 40 P > BLA Fluoresene intensity 50 BLA Stritum 0 Trer TH ChR2EYFP mpfc 0 % ChR2EYFP mong tred DA neurons % ChR2EYFP mong TH mpfc 0 Tred Lterl Figure S3. ChR2 expression is uniform ross dopminergi neurons with different projetion trgets. A reent study found lower levels of DAT in dopminergi neurons projeting to prefrontl ortex, nuleus umens ore, nd solterl mygdl versus those projeting to lterl nuleus umens shell nd dorsolterl stritum16. Beuse Cre expression in the DATCre mouse is under the ontrol of the DAT gene promoter, this ould hve ised ChR2 expression towrd ells with high DAT promoter tivity. To onfirm tht our reordings were not ised towrd dopminergi neurons with prtiulr projetion trget, we injeted fluorogold, retrogrde trer, into the prefrontl ortex, stritum, or solterl mygdl in AAVFLEXChR2injeted DATCre mie, nd ounted the proportion of THexpressing neurons tht lso expressed fluorogold nd ChR2., Fluorogold tring from medil prefrontl ortex (mpfc, left), stritum (middle), nd solterl mygdl (BLA, right) with stins for ell nulei (ToPro3, lue), TH (red), ChR2EYFP (green), fluorogold (white), nd their overly. Sle rs: 1 mm (left) nd 50 μm (right)., The infetion effiieny of dopminergi neurons with identified projetion to mpfc, stritum nd BLA ws similr to the overll infetion effiieny mesured throughout (Fig. S2). The perentge of neurons tripleleled y trer, TH, nd ChR2EYFP ws similr ross projetion trget sites, suggesting tht virusmedited ChR2 expression did not preferentilly trget supopultion of dopminergi neurons (mpfc, n = 67, stritum, n = 145, BLA, n = 35)., Dopminergi neurons with high DAT expression re minly found in the lterl extent of 21, while low DAT expressing neurons re distriuted throughout the medil to lterl extent of. Consistent with the finding in (), the virl infetion effiieny ws similr long the medillterl xis of (n = 39). d, To evlute possile differenes in ellulr ChR2 expression levels, we mesured the reltive ChR2EYFP fluoresene intensity over kground in dopminergi neurons projeting to mpfc, BLA or stritum nd dopminergi neurons in the lterl (prrhil pigmented nuleus). ChR2EYFP expression ws similr in ll nlysed dopminergi neurons (n = 25 for eh ondition). 5
6 Pek mplitude wire 3 (mv) d 0 10 g Unit Men (ms) Pek mplitude wire 2 (mv) Spike Lteny P(spike) SD (ms) Frequeny (Hz) e P(spike) Spikes Frequeny (Hz) f Spike lteny (ms) Lteny (ms) Frequeny (Hz) k Spikes/s m GABAergi exmple 1 PC PC1 o PC3 l n Bseline spikes/s uroc (vs. seline) 1 (Inrese) 0 (Derese) Type I Type II Type III Spike durtion (ms) Time (ms) h Spike Lteny Men (ms) SD (ms) i P(spike) Frequeny (Hz) Time (ms) j Lteny (ms) Frequeny (Hz) Dopminergi GABAergi 0.2 mv 1 ms Figure S4. Identifition of lightresponsive neurons., Isoltion of the neuron in Fig. 3. Binned stterplot shows pek mplitude of spike wveforms from two wires of the tetrode. Isolted unit is the upper luster. The lower luster is noise., Proility of spike (for the seond through tenth pulses in eh trin) s funtion of stimultion frequeny for this neuron., Spike lteny reltive to light onset for this neuron. d, Histogrm of men (left) nd SD (right) spike lteny to light stimultion for 26 identified dopminergi neurons. e, Proility of spike s funtion of stimultion frequeny for eh dopminergi neuron (grey) nd the men ross dopminergi neurons (yn). f, Men ± SEM spike lteny s funtion of stimultion frequeny. g, Response from GABAergi neuron to 5 repetitions of 10 Hz (left) or 20 Hz (right) light stimultion (yn rs). Tiks represent spikes. h, Histogrm of men (left) nd SD (right) spike lteny to light stimultion for 17 identified GABAergi neurons. i, Proility of spike s funtion of stimultion frequeny for eh GABAergi neuron (grey) nd the men ross GABAergi neurons (yn). j, Men ± SEM spike lteny s funtion of stimultion frequeny. k, Response pttern of n exmple identified GABAergi neuron. l, Temporl response profiles of identified GABAergi neurons. Conventions re s in Fig. 2. m, The first three prinipl omponents of the uroc urves of ll neurons from Fig. 2 (smll points) nd from identified GABAergi neurons (lrge points), using the model fit from Fig. 2. Eh GABAergi neuron fell within 95% onfidene intervls of the Type II luster defined in DAT Cre mie. n, Bseline firing rte vs. spike durtion for neurons of eh type with density histogrms in the mrgins. Spike durtion ws lulted s the time t whih the voltge ws signifintly different from seline (1 ms of prespike voltge). o, Men spontneous (lk) nd lightevoked (yn) spike wveforms from 26 identified dopminergi neurons nd 17 identified GABAergi neurons. 6
7 Liks/s Liks/s Dy Figure S5., Liking ehviour from representtive experimentl session from VgtCre mouse. Blk rs indite CS nd US delivery. Shded regions round lik tres denote SEM., men ± SEM liks during the dely etween CS nd US s funtion of dys of the experiment ross VgtCre nimls. 7
8 d % hnge fter irpuff Firing rte (spikes/s) Type I % hnge fter light % hnge fter rewrd omission Big rewrd Smll rewrd Nothing Punishment % hnge fter light 4 Time (s) CS US index % hnge fter light Type I Type II Type III DATCre P< VgtCre % hnge fter light % hnge fter light % hnge fter light Figure S6. Puttive synpti effets of ChR2 stimultion., Firing rtes from Type I neuron in VgtCre mouse., Response of the neuron to 12 trils of 10 Hz light pulses (yn rs). The neuron ws inhiited y GABAergi stimultion., Stter plots of % hnge (mximl mgnitude of hnge in the 520 ms following light pulses) in firing rte fter irpuff, rewrd omission, nd CSUS index vs. % hnge (mximl mgnitude of hnge) in firing rte fter light stimultion in 28 Type I neurons from VgtCre mie. The 11 neurons for whih light stimultion hd signifint effet re shown in lk (Wiloxon rnk sum test, P < 0.05). There ws signifint orreltion etween % hnge in firing rte fter irpuff nd % hnge in firing rte fter light stimultion ross the popultion (r = 0.59, P < 0.001) nd for the 11 neurons with signifint response to light stimultion (r = 0.86, P < 0.001). d, % firing rte hnges from seline in the 520 ms following ll light pulses in DATCre (top row) nd VgtCre (ottom row) mie for eh neuron type. 8
9 CS firing rte (spikes/s) Dely firing rte (spikes/s) US firing rte (spikes/s) GABAergi Dopminergi uroc (rewrded vs. omitted) Type III Punishment CS US index Nothing Smll rewrd Big rewrd uroc (seline vs. omitted) Punishment Nothing Smll rewrd CS US index Big rewrd d uroc (irpuff vs. seline) Punishment Rewrd omission Nothing Smll rewrd Big rewrd CS US index e uroc (rewrded vs. omitted) uroc (irpuff vs. seline) Figure S7., Men firing rtes for identified dopminergi (top row), GABAergi (middle row), nd Type III (ottom row) neurons during CS (left olumn), dely etween CS nd US (middle olumn), nd 500 ms fter US onset (right olumn). Eh neuron is plotted in grey with the men nd SEM overlid. Individul dopminergi neurons re plotted s funtion of their CSUS index, with red inditing lrge CSUS index (i.e., higher firing rte for CS vs. US), lue inditing smll CSUS index., uroc vlues for rewrd present ompred to rewrd sent versus CSUS index. There ws signifint negtive orreltion (r = 0.51, P < 0.05) tht disppered with leverge nlysis, inditing tht the orreltion ws driven mostly y one or two neurons., uroc vlues for seline ompred to rewrd sent versus CSUS index. There ws no signifint orreltion. d, uroc vlues for rewrd present ompred to rewrd sent versus uroc vlues for irpuff ompred to seline. There ws no signifint orreltion. e, uroc vlues for irpuff ompred to seline versus CSUS index. There ws no signifint orreltion. 9
10 Dopmine Type II Type III Rewrded uroc (vs. seline) 1.0 X X X 0.5 Omitted 0.0 Dopminergi neurons P< uroc (omitted vs. seline) Firing rte (spikes/s) Type III Dopmine Type II Type III uroc (rewrded vs. omitted) uroc (Rewrded vs. omitted) GABA 0.0 Figure S8. Response profiles of ll neurons during rewrdomitted trils., Firing ptterns during igrewrd trils in whih rewrd ws delivered (top) nd omitted (ottom). Firing rte hnges from seline were quntified using the uroc urve. Vlues were omputed etween eh neuron's tivity ross time nd its seline tivity. Yellow: inrese from seline, yn: derese from seline., Histogrm of uroc vlues during the rewrd omission period reltive to seline for dopminergi neurons (left) nd exmple Type III neuron nd histogrm of uroc vlues for rewrded versus omitted trils., Differene etween rewrded nd rewrdomitted trils for igrewrd trils for identified dopminergi neurons, unidentified DATCre Types II nd III neurons, nd identified GABAergi neurons. uroc vlues were omputed etween rewrdpresent nd rewrdsent trils. Eh row represents one neuron. Yellow: rewrded > omitted, yn: rewrded < omitted. 10
11 Type I Type II uroc (vs. seline) 1.0 Type III Figure S9. Response profiles of ll neurons during irpuff trils. uroc urves for punishment trils reltive to seline tivity. 11
12 d Firing rte (spikes/s) Firing rte (spikes/s) Type I: dopminergi Type I: unidentified Type II r CS r US r CS r US Big rewrd Smll rewrd Nothing Punishment f g h CS firing rte (spikes/s) CS slope Rewrd size (µl) Dopminergi P<0.05 CS slope US firing rte (spikes/s) Rewrd size (µl) Dopminergi US slope Spikes/s e Spikes/s Dopminergi GABAergi Spikes/s i US slope Dopminergi Dely slope GABAergi Dely slope Time of hlf mximum firing rte (s odour) Figure S10. Firing ptterns of more exmple neurons nd CS nd US responses in dopminergi neurons., Exmples of firing rtes from identified nd unidentified Type I neurons., Averge firing rtes from 26 identified dopminergi neurons nd 23 unidentified Type I neurons., Exmples of firing rtes from Type II neurons. d, Averge firing rtes from the lowest, middle, nd upper third of the CSUS index histogrm in Fig. 4 (reprodued here). e, The time of hlfmximum firing rte during igrewrd trils from odour onset to rewrd onset. Identified GABAergi neuron firing rtes slowly rose to pek, while identified dopminergi neuron firing rtes peked during the CS. f, Firing rtes for dopminergi neurons during CS nd US. g, Regression slopes of the firing rtes versus rewrd size during CS nd US for dopminergi neurons during CS nd. h, Slope vlues for eh dopminergi neuron during CS nd US. i, Slope vlues during the dely etween CS nd US. While the dely tivity of GABAergi neurons ws prmetrilly modulted y the vlue of rewrd, none of identified dopminergi neurons showed suh modultion. Unidentified Type II neurons showed similr modultion y rewrd vlue s GABAergi neurons (43/47 unidentified Type II neurons showed signifint delyperiod slope vlues nd 40/47 showed signifint differenes etween no, smll nd igrewrd trils, P < 0.001). 12
13 Dopminergi output CS Synpti inputs Cue Exittory Atul rewrd Rewrd expettion Exittory Inhiitory Expettion Inhiition Exittion PFC Ctx Str Amy Hipp RPE Expettion version Aversion LH Expettion DAergi GABAergi Expettion Str Type III PPN Figure S11. Proposed RPE model nd iruit digrm., A synpti model of RPE lultion (fter Houk et l., 1995). Dopminergi spikes re result of exittory inputs out rewrdprediting ues nd tul rewrd, nd inhiitory inputs out rewrd expettion., Shemti intertion of dopminergi (DAergi) nd GABAergi neurons. reeives rewrdexpettion input from prefrontl ortex (PFC, inluding oritofrontl ortex), stritum (str) nd pedunulopontine nuleus (PPN). reeives inputs out versive stimuli from lterl henul (LH). GABAergi neurons integrte informtion out rewrd expettion nd versive stimuli nd dopminergi neurons projet RPE signls to ortex (tx), stritum, mygdl (my), hippompus (hipp), nd elsewhere. Exmple firing rtes from eh type of neuron we reorded re shown. We hve omitted mny other res known to e importnt in this iruit (e.g., rostromedil tegmentl nuleus). See text for detils. 13
14 DAT RN SN SNr RN SN SNr RN SN SNr Vgt RN SN SNr RN SN SNr RN SN SNr Bregm: 3.00 mm Bregm: 3.50 mm Bregm: 3.60 mm 1 mm Figure S12. Histologil reonstrution of reording sites (red irles). Leled strutures: red nuleus (RN), sustnti nigr prs ompt (SN), sustnti nigr prs retiult (SNr),. 14
15 P(spike t 50 Hz light stimultion) ms Isoltion qulity (L rtio) 0.3 mv Figure S13. Dopminergi neurons follow highfrequeny light stimultion., Five onseutive trils of 50 Hz light stimultion from dopminergi neuron., Proility of following 50 Hz stimultion s funtion of isoltion qulity, mesured using the Lrtio. Smller vlues indite etter isoltion. The Lrtio for the exmple neuron is
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